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Roger W Craig PhD

TitleProfessor
InstitutionUniversity of Massachusetts Medical School
DepartmentRadiology
AddressUniversity of Massachusetts Medical School
55 Lake Avenue North
Worcester MA 01655
Phone508-856-2474
vCardDownload vCard
    Other Positions
    InstitutionUMMS - School of Medicine
    DepartmentRadiology

    InstitutionUMMS - Graduate School of Biomedical Sciences
    DepartmentCell Biology


    Collapse Biography 
    Collapse education and training
    University of Sydney, Sydney, NSW, AustraliaBSCZoology
    King's College London, London, , United KingdomPHDBiophysics

    Collapse Overview 
    Collapse overview

    Molecular Structure, Dynamics, and Contractile Mechanism of Muscle


    We use state-of-the-art electron microscopic techniques to understand how muscles contract. By studying the molecular structures of the actin and myosin filaments, whose interaction is responsible for contraction, we can elucidate the molecular mechanism of force generation and the processes responsible for regulating contraction. We are investigating systems as diverse as the rapidly contracting striated muscles of the skeleton and heart, and the smooth muscles of the internal organs (e.g. blood vessels), which are specialized to contract slowly and to maintain tension over long periods of time. These studies are adding to our basic understanding of muscle function, and also providing a structural basis for understanding muscle diseases caused by malfunction in the actin or myosin filaments.


    Techniques: high resolution electron microscopy, 3D reconstruction, and atomic fitting


    To decipher these filament structures in three dimensions at the molecular level, we use high resolution electron microscopy combined with computer image reconstruction. Specimens are observed by negative staining or cryo-electron microscopy, and 3D reconstructions of filaments are computed using helical or single particle methods. Atomic level detail is achieved by computationally 'fitting' atomic structures of filament subunits into the reconstruction. To study dynamic changes in filament structure that occur in active muscle, we have developed methods for capturing transient structural intermediates on the millisecond time scale for observation by EM.


    Myosin filaments


    Using these approaches we have recently achieved a major breakthrough in defining the 3D configuration of the key energy-transducing molecules, the myosin heads, on the surface of striated muscle myosin filaments (Woodhead et al., 2005). These results show for the first time, and in atomic detail, how myosin molecules are switched 'off', bringing about relaxation of muscle. The results suggest that the structure we observe is common to muscles of animals throughout most of the animal kingdom, and they provide a basis for understanding how these filaments are activated in contracting muscle. Our results also reveal for the first time how the tails of the myosin molecules are packed into the backbone of the thick filament, forming small 'subfilaments' that themselves assemble to form the thick filament core. This provides key background information for understanding how myosin filaments assemble in the cell.


    Actin filaments


    We have also made the first direct observations of how the protein tropomyosin, on the actin filament, regulates contraction by sterically blocking sites of myosin head attachment on actin filaments (Lehman et al., 1994; Xu et al., 1999; Pirani et al., 2005). We are currently determining the organization of the Ca2+-sensitive regulatory complex, troponin, on the thin filament, and how this changes on Ca2+ activation. These studies are revealing in atomic detail the molecular dynamics regulating muscle contraction.


    Smooth muscle


    In addition to our work on striated muscle, we have also shown that the myosin filaments of smooth muscle have a unique 'side-polar' structure, different from the helical organization in striated muscle. This structure helps to explain the characteristic ability of smooth muscles to undergo high degrees of shortening (Xu et al., 1996). Actin filaments from smooth muscle also differ from those in striated muscle, and we have gained new insights into their functioning in terms of the organization of their associated regulatory proteins (Hodgkinson et al., 1997; Lehman et al., 1997).


    Current studies


    We are currently determining the head organization in striated muscle myosin filaments from several key organisms, to test the generality of our model of the off state, and to determine whether subfilaments are a common feature of different species. We are imaging filaments at higher resolution to determine further details of their structure, and are carrying out tomographic studies of smooth muscle filaments to determine the three-dimensional details of their side-polar structure. In our studies of thin filaments, we are developing new methods of 3D reconstruction to reveal further details of the organization of troponin on actin, and we are combining the reconstructions with crystallographic structures of the thin filament components to produce a 3D thin filament model at the atomic level.


     


    Myosin figure
     

    Figure 1. 3D reconstruction and atomic fitting of (thick) myosin filament (from Woodhead et al., 2005). Left: 3D reconstruction showing arrangement of myosin heads on filament surface, and subfilaments running parallel to axis in filament backbone. Right: fitting of atomic structure of myosin heads (space-filling colored balls) into reconstruction of one pair of heads. The fitting reveals that the two heads interact with each other, preventing interaction with actin and thereby switching contraction off.

     

    Actin figure


    Figure 2. 3D reconstruction and atomic fitting of thin filament. Left: 3D reconstruction based on cryo images of thin filaments (from Xu et al., 1999). Actin in gold, tropomyosin in red (myosin blocking position), and green (non-blocking position). Right: fitting of actin atomic structure (yellow, α-carbon chain) into reconstruction of one actin subunit (blue wire). Highlighted in orange are amino acid clusters on actin that are blocked by tropomyosin in blocking position (white arrow). From Vibert et al., 1997.



    Collapse Rotation Projects

    Potential Rotation Projects

    Project #1: Lipid-Layer Protein Crystallization for Electron Microscopy.While individual protein molecules can be readily visualized by EM, structural information is greatly enhanced if the molecules can by crystallized into 2-dimensional ordered arrays. Methods for achieving this are well established, making use of lipid monolayers at an air-water interface.

    1. Follow literature methods to crystallize "standard" proteins using the lipid-layer method.
    2. Observe results by electron microscopy following negative staining.
    3. If time permits, carry out preliminary image processing of micrographs and/or crystallization of unknown proteins. Techniques to be learned: lipid layer crystallization methods; grid preparation; use of electron microscope; image processing.


    Collapse Post Docs

    A postdoctoral position is available to study in this laboratory. Contact Dr. Craig for additional details.


    Collapse Bibliographic 
    Collapse selected publications
    Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Faculty can login to make corrections and additions.
    List All   |   Timeline
    1. Kensler RW, Craig R, Moss RL. Phosphorylation of cardiac myosin binding protein C releases myosin heads from the surface of cardiac thick filaments. Proc Natl Acad Sci U S A. 2017 Feb 21; 114(8):E1355-E1364. PMID: 28167762.
      View in: PubMed
    2. Previs MJ, Mun JY, Michalek AJ, Previs SB, Gulick J, Robbins J, Warshaw DM, Craig R. Phosphorylation and calcium antagonistically tune myosin-binding protein C's structure and function. Proc Natl Acad Sci U S A. 2016 Mar 22; 113(12):3239-44. PMID: 26908872.
      View in: PubMed
    3. Kirk JA, Chakir K, Lee KH, Karst E, Holewinski RJ, Pironti G, Tunin RS, Pozios I, Abraham TP, de Tombe P, Rockman HA, Van Eyk JE, Craig R, Farazi TG, Kass DA. Pacemaker-induced transient asynchrony suppresses heart failure progression. Sci Transl Med. 2015 Dec 23; 7(319):319ra207. PMID: 26702095.
      View in: PubMed
    4. Mun JY, Kensler RW, Harris SP, Craig R. The cMyBP-C HCM variant L348P enhances thin filament activation through an increased shift in tropomyosin position. J Mol Cell Cardiol. 2016 Feb; 91:141-7. PMID: 26718724.
      View in: PubMed
    5. Yang S, Woodhead JL, Zhao FQ, Sulbarán G, Craig R. An approach to improve the resolution of helical filaments with a large axial rise and flexible subunits. J Struct Biol. 2016 Jan; 193(1):45-54. PMID: 26592473.
      View in: PubMed
    6. Sulbarán G, Alamo L, Pinto A, Márquez G, Méndez F, Padrón R, Craig R. An invertebrate smooth muscle with striated muscle myosin filaments. Proc Natl Acad Sci U S A. 2015 Oct 20; 112(42):E5660-8. PMID: 26443857.
      View in: PubMed
    7. Woodhead JL, Craig R. Through Thick and Thin--Interfilament Communication in Muscle. Biophys J. 2015 Aug 18; 109(4):665-7. PMID: 26287618.
      View in: PubMed
    8. Previs MJ, Prosser BL, Mun JY, Previs SB, Gulick J, Lee K, Robbins J, Craig R, Lederer WJ, Warshaw DM. Myosin-binding protein C corrects an intrinsic inhomogeneity in cardiac excitation-contraction coupling. Sci Adv. 2015; 1(1). PMID: 25839057.
      View in: PubMed
    9. Lee K, Harris SP, Sadayappan S, Craig R. Orientation of myosin binding protein C in the cardiac muscle sarcomere determined by domain-specific immuno-EM. J Mol Biol. 2015 Jan 30; 427(2):274-86. PMID: 25451032.
      View in: PubMed
    10. Yang S, Barbu-Tudoran L, Orzechowski M, Craig R, Trinick J, White H, Lehman W. Three-dimensional organization of troponin on cardiac muscle thin filaments in the relaxed state. Biophys J. 2014 Feb 18; 106(4):855-64. PMID: 24559988.
      View in: PubMed
    11. Mun JY, Previs MJ, Yu HY, Gulick J, Tobacman LS, Beck Previs S, Robbins J, Warshaw DM, Craig R. Myosin-binding protein C displaces tropomyosin to activate cardiac thin filaments and governs their speed by an independent mechanism. Proc Natl Acad Sci U S A. 2014 Feb 11; 111(6):2170-5. PMID: 24477690.
      View in: PubMed
    12. Craig R, Lee KH, Mun JY, Torre I, Luther PK. Structure, sarcomeric organization, and thin filament binding of cardiac myosin-binding protein-C. Pflugers Arch. 2014 Mar; 466(3):425-31. PMID: 24413886.
      View in: PubMed
    13. Sulbarán G, Biasutto A, Alamo L, Riggs C, Pinto A, Méndez F, Craig R, Padrón R. Different head environments in tarantula thick filaments support a cooperative activation process. Biophys J. 2013 Nov 5; 105(9):2114-22. PMID: 24209856.
      View in: PubMed
    14. Lin B, Govindan S, Lee K, Zhao P, Han R, Runte KE, Craig R, Palmer BM, Sadayappan S. Cardiac myosin binding protein-C plays no regulatory role in skeletal muscle structure and function. PLoS One. 2013; 8(7):e69671. PMID: 23936073.
      View in: PubMed
    15. Woodhead JL, Zhao FQ, Craig R. Structural basis of the relaxed state of a Ca2+-regulated myosin filament and its evolutionary implications. Proc Natl Acad Sci U S A. 2013 May 21; 110(21):8561-6. PMID: 23650385.
      View in: PubMed
    16. Craig R. Isolation, electron microscopy and 3D reconstruction of invertebrate muscle myofilaments. Methods. 2012 Jan; 56(1):33-43. PMID: 22155190.
      View in: PubMed
    17. Luther PK, Craig R. Modulation of striated muscle contraction by binding of myosin binding protein C to actin. Bioarchitecture. 2011 Nov 1; 1(6):277-283. PMID: 22545180.
      View in: PubMed
    18. Brito R, Alamo L, Lundberg U, Guerrero JR, Pinto A, Sulbarán G, Gawinowicz MA, Craig R, Padrón R. A molecular model of phosphorylation-based activation and potentiation of tarantula muscle thick filaments. J Mol Biol. 2011 Nov 18; 414(1):44-61. PMID: 21959262.
      View in: PubMed
    19. Luther PK, Winkler H, Taylor K, Zoghbi ME, Craig R, Padrón R, Squire JM, Liu J. Direct visualization of myosin-binding protein C bridging myosin and actin filaments in intact muscle. Proc Natl Acad Sci U S A. 2011 Jul 12; 108(28):11423-8. PMID: 21705660.
      View in: PubMed
    20. Mun JY, Gulick J, Robbins J, Woodhead J, Lehman W, Craig R. Electron microscopy and 3D reconstruction of F-actin decorated with cardiac myosin-binding protein C (cMyBP-C). J Mol Biol. 2011 Jul 8; 410(2):214-25. PMID: 21601575.
      View in: PubMed
    21. Li XE, Tobacman LS, Mun JY, Craig R, Fischer S, Lehman W. Tropomyosin position on F-actin revealed by EM reconstruction and computational chemistry. Biophys J. 2011 Feb 16; 100(4):1005-13. PMID: 21320445.
      View in: PubMed
    22. Badyal SK, Basran J, Bhanji N, Kim JH, Chavda AP, Jung HS, Craig R, Elliott PR, Irvine AF, Barsukov IL, Kriajevska M, Bagshaw CR. Mechanism of the Ca²+-dependent interaction between S100A4 and tail fragments of nonmuscle myosin heavy chain IIA. J Mol Biol. 2011 Jan 28; 405(4):1004-26. PMID: 21110983.
      View in: PubMed
    23. Galinska A, Hatch V, Craig R, Murphy AM, Van Eyk JE, Wang CL, Lehman W, Foster DB. The C terminus of cardiac troponin I stabilizes the Ca2+-activated state of tropomyosin on actin filaments. Circ Res. 2010 Mar 05; 106(4):705-11. PMID: 20035081.
      View in: PubMed
    24. Cammarato A, Craig R, Lehman W. Electron microscopy and three-dimensional reconstruction of native thin filaments reveal species-specific differences in regulatory strand densities. Biochem Biophys Res Commun. 2010 Jan 1; 391(1):193-7. PMID: 19900412.
      View in: PubMed
    25. Umeki N, Jung HS, Watanabe S, Sakai T, Li XD, Ikebe R, Craig R, Ikebe M. The tail binds to the head-neck domain, inhibiting ATPase activity of myosin VIIA. Proc Natl Acad Sci U S A. 2009 May 26; 106(21):8483-8. PMID: 19423668.
      View in: PubMed
    26. Lehman W, Galinska-Rakoczy A, Hatch V, Tobacman LS, Craig R. Structural basis for the activation of muscle contraction by troponin and tropomyosin. J Mol Biol. 2009 May 15; 388(4):673-81. PMID: 19341744.
      View in: PubMed
    27. Zhu J, Sun Y, Zhao FQ, Yu J, Craig R, Hu S. Analysis of tarantula skeletal muscle protein sequences and identification of transcriptional isoforms. BMC Genomics. 2009 Mar 19; 10:117. PMID: 19298669.
      View in: PubMed
    28. Zhao FQ, Craig R, Woodhead JL. Head-head interaction characterizes the relaxed state of Limulus muscle myosin filaments. J Mol Biol. 2009 Jan 16; 385(2):423-31. PMID: 18976661.
      View in: PubMed
    29. Alamo L, Wriggers W, Pinto A, Bártoli F, Salazar L, Zhao FQ, Craig R, Padrón R. Three-dimensional reconstruction of tarantula myosin filaments suggests how phosphorylation may regulate myosin activity. J Mol Biol. 2008 Dec 26; 384(4):780-97. PMID: 18951904.
      View in: PubMed
    30. Luther PK, Bennett PM, Knupp C, Craig R, Padrón R, Harris SP, Patel J, Moss RL. Understanding the organisation and role of myosin binding protein C in normal striated muscle by comparison with MyBP-C knockout cardiac muscle. J Mol Biol. 2008 Dec 5; 384(1):60-72. PMID: 18817784.
      View in: PubMed
    31. Jung HS, Craig R. Ca2+ -induced tropomyosin movement in scallop striated muscle thin filaments. J Mol Biol. 2008 Nov 14; 383(3):512-9. PMID: 18775725.
      View in: PubMed
    32. Zhao FQ, Padrón R, Craig R. Blebbistatin stabilizes the helical order of myosin filaments by promoting the switch 2 closed state. Biophys J. 2008 Oct; 95(7):3322-9. PMID: 18599626.
      View in: PubMed
    33. Zhao FQ, Craig R. Millisecond time-resolved changes occurring in Ca2+-regulated myosin filaments upon relaxation. J Mol Biol. 2008 Aug 29; 381(2):256-60. PMID: 18585394.
      View in: PubMed
    34. Jung HS, Komatsu S, Ikebe M, Craig R. Head-head and head-tail interaction: a general mechanism for switching off myosin II activity in cells. Mol Biol Cell. 2008 Aug; 19(8):3234-42. PMID: 18495867.
      View in: PubMed
    35. Galinska-Rakoczy A, Engel P, Xu C, Jung H, Craig R, Tobacman LS, Lehman W. Structural basis for the regulation of muscle contraction by troponin and tropomyosin. J Mol Biol. 2008 Jun 20; 379(5):929-35. PMID: 18514658.
      View in: PubMed
    36. Zoghbi ME, Woodhead JL, Moss RL, Craig R. Three-dimensional structure of vertebrate cardiac muscle myosin filaments. Proc Natl Acad Sci U S A. 2008 Feb 19; 105(7):2386-90. PMID: 18252826.
      View in: PubMed
    37. Li XD, Jung HS, Wang Q, Ikebe R, Craig R, Ikebe M. The globular tail domain puts on the brake to stop the ATPase cycle of myosin Va. Proc Natl Acad Sci U S A. 2008 Jan 29; 105(4):1140-5. PMID: 18216256.
      View in: PubMed
    38. Lehman W, Craig R. Tropomyosin and the steric mechanism of muscle regulation. Adv Exp Med Biol. 2008; 644:95-109. PMID: 19209816.
      View in: PubMed
    39. Li XD, Jung HS, Mabuchi K, Craig R, Ikebe M. The globular tail domain of myosin Va functions as an inhibitor of the myosin Va motor. J Biol Chem. 2006 Aug 4; 281(31):21789-98. PMID: 16757473.
      View in: PubMed
    40. Poole KJ, Lorenz M, Evans G, Rosenbaum G, Pirani A, Craig R, Tobacman LS, Lehman W, Holmes KC. A comparison of muscle thin filament models obtained from electron microscopy reconstructions and low-angle X-ray fibre diagrams from non-overlap muscle. J Struct Biol. 2006 Aug; 155(2):273-84. PMID: 16793285.
      View in: PubMed
    41. Craig R, Woodhead JL. Structure and function of myosin filaments. Curr Opin Struct Biol. 2006 Apr; 16(2):204-12. PMID: 16563742.
      View in: PubMed
    42. Pirani A, Vinogradova MV, Curmi PM, King WA, Fletterick RJ, Craig R, Tobacman LS, Xu C, Hatch V, Lehman W. An atomic model of the thin filament in the relaxed and Ca2+-activated states. J Mol Biol. 2006 Mar 31; 357(3):707-17. PMID: 16469331.
      View in: PubMed
    43. Woodhead JL, Zhao FQ, Craig R, Egelman EH, Alamo L, Padrón R. Atomic model of a myosin filament in the relaxed state. Nature. 2005 Aug 25; 436(7054):1195-9. PMID: 16121187.
      View in: PubMed
    44. Cammarato A, Craig R, Sparrow JC, Lehman W. E93K charge reversal on actin perturbs steric regulation of thin filaments. J Mol Biol. 2005 Apr 15; 347(5):889-94. PMID: 15784249.
      View in: PubMed
    45. Pirani A, Xu C, Hatch V, Craig R, Tobacman LS, Lehman W. Single particle analysis of relaxed and activated muscle thin filaments. J Mol Biol. 2005 Feb 25; 346(3):761-72. PMID: 15713461.
      View in: PubMed
    46. Gong H, Hatch V, Ali L, Lehman W, Craig R, Tobacman LS. Mini-thin filaments regulated by troponin-tropomyosin. Proc Natl Acad Sci U S A. 2005 Jan 18; 102(3):656-61. PMID: 15644437.
      View in: PubMed
    47. Foster DB, Huang R, Hatch V, Craig R, Graceffa P, Lehman W, Wang CL. Modes of caldesmon binding to actin: sites of caldesmon contact and modulation of interactions by phosphorylation. J Biol Chem. 2004 Dec 17; 279(51):53387-94. PMID: 15456752.
      View in: PubMed
    48. Zoghbi ME, Woodhead JL, Craig R, Padrón R. Helical order in tarantula thick filaments requires the "closed" conformation of the myosin head. J Mol Biol. 2004 Sep 24; 342(4):1223-36. PMID: 15351647.
      View in: PubMed
    49. Cammarato A, Hatch V, Saide J, Craig R, Sparrow JC, Tobacman LS, Lehman W. Drosophila muscle regulation characterized by electron microscopy and three-dimensional reconstruction of thin filament mutants. Biophys J. 2004 Mar; 86(3):1618-24. PMID: 14990488.
      View in: PubMed
    50. Lehman W, Craig R. The structure of the vertebrate striated muscle thin filament: a tribute to the contributions of Jean Hanson. J Muscle Res Cell Motil. 2004; 25(6):455-66. PMID: 15630610.
      View in: PubMed
    51. Lehman W, Craig R, Kendrick-Jones J, Sutherland-Smith AJ. An open or closed case for the conformation of calponin homology domains on F-actin? J Muscle Res Cell Motil. 2004; 25(4-5):351-8. PMID: 15548864.
      View in: PubMed
    52. Luther PK, Padrón R, Ritter S, Craig R, Squire JM. Heterogeneity of Z-band structure within a single muscle sarcomere: implications for sarcomere assembly. J Mol Biol. 2003 Sep 5; 332(1):161-9. PMID: 12946354.
      View in: PubMed
    53. Sutherland-Smith AJ, Moores CA, Norwood FL, Hatch V, Craig R, Kendrick-Jones J, Lehman W. An atomic model for actin binding by the CH domains and spectrin-repeat modules of utrophin and dystrophin. J Mol Biol. 2003 May 23; 329(1):15-33. PMID: 12742015.
      View in: PubMed
    54. Zhao FQ, Craig R. Ca2+ causes release of myosin heads from the thick filament surface on the milliseconds time scale. J Mol Biol. 2003 Mar 14; 327(1):145-58. PMID: 12614614.
      View in: PubMed
    55. Zhao FQ, Craig R. Capturing time-resolved changes in molecular structure by negative staining. J Struct Biol. 2003 Jan; 141(1):43-52. PMID: 12576019.
      View in: PubMed
    56. Tobacman LS, Nihli M, Butters C, Heller M, Hatch V, Craig R, Lehman W, Homsher E. The troponin tail domain promotes a conformational state of the thin filament that suppresses myosin activity. J Biol Chem. 2002 Aug 2; 277(31):27636-42. PMID: 12011043.
      View in: PubMed
    57. Tonino P, Simon M, Craig R. Mass determination of native smooth muscle myosin filaments by scanning transmission electron microscopy. J Mol Biol. 2002 May 10; 318(4):999-1007. PMID: 12054797.
      View in: PubMed
    58. Craig R, Lehman W. The ultrastructural basis of actin filament regulation. Results Probl Cell Differ. 2002; 36:149-69. PMID: 11892278.
      View in: PubMed
    59. Hidalgo C, Padrón R, Horowitz R, Zhao FQ, Craig R. Purification of native myosin filaments from muscle. Biophys J. 2001 Nov; 81(5):2817-26. PMID: 11606293.
      View in: PubMed
    60. Craig R, Lehman W. Crossbridge and tropomyosin positions observed in native, interacting thick and thin filaments. J Mol Biol. 2001 Aug 31; 311(5):1027-36. PMID: 11531337.
      View in: PubMed
    61. Ikebe M, Komatsu S, Woodhead JL, Mabuchi K, Ikebe R, Saito J, Craig R, Higashihara M. The tip of the coiled-coil rod determines the filament formation of smooth muscle and nonmuscle myosin. J Biol Chem. 2001 Aug 10; 276(32):30293-300. PMID: 11395487.
      View in: PubMed
    62. Hidalgo C, Craig R, Ikebe M, Padrón R. Mechanism of phosphorylation of the regulatory light chain of myosin from tarantula striated muscle. J Muscle Res Cell Motil. 2001; 22(1):51-9. PMID: 11563549.
      View in: PubMed
    63. Rosol M, Lehman W, Craig R, Landis C, Butters C, Tobacman LS. Three-dimensional reconstruction of thin filaments containing mutant tropomyosin. Biophys J. 2000 Feb; 78(2):908-17. PMID: 10653803.
      View in: PubMed
    64. Wang L, Zhou P, Craig RW, Lu L. Protection from cell death by mcl-1 is mediated by membrane hyperpolarization induced by K(+) channel activation. J Membr Biol. 1999 Nov 15; 172(2):113-20. PMID: 10556359.
      View in: PubMed
    65. Xu C, Craig R, Tobacman L, Horowitz R, Lehman W. Tropomyosin positions in regulated thin filaments revealed by cryoelectron microscopy. Biophys J. 1999 Aug; 77(2):985-92. PMID: 10423443.
      View in: PubMed
    66. Bangs P, Burke B, Powers C, Craig R, Purohit A, Doxsey S. Functional analysis of Tpr: identification of nuclear pore complex association and nuclear localization domains and a role in mRNA export. J Cell Biol. 1998 Dec 28; 143(7):1801-12. PMID: 9864356.
      View in: PubMed
    67. Xu JQ, Gillis JM, Craig R. Polymerization of myosin on activation of rat anococcygeus smooth muscle. J Muscle Res Cell Motil. 1997 Jun; 18(3):381-93. PMID: 9172080.
      View in: PubMed
    68. Zhan Q, Bieszczad CK, Bae I, Fornace AJ, Craig RW. Induction of BCL2 family member MCL1 as an early response to DNA damage. Oncogene. 1997 Mar 6; 14(9):1031-9. PMID: 9070651.
      View in: PubMed
    69. Xu JQ, Harder BA, Uman P, Craig R. Myosin filament structure in vertebrate smooth muscle. J Cell Biol. 1996 Jul; 134(1):53-66. PMID: 8698822.
      View in: PubMed
    70. Lehman W, Vibert P, Uman P, Craig R. Steric-blocking by tropomyosin visualized in relaxed vertebrate muscle thin filaments. J Mol Biol. 1995 Aug 11; 251(2):191-6. PMID: 7643394.
      View in: PubMed
    71. Yang T, Kozopas KM, Craig RW. The intracellular distribution and pattern of expression of Mcl-1 overlap with, but are not identical to, those of Bcl-2. J Cell Biol. 1995 Mar; 128(6):1173-84. PMID: 7896880.
      View in: PubMed
    72. Craig RW. The bcl-2 gene family. Semin Cancer Biol. 1995 Feb; 6(1):35-43. PMID: 7548840.
      View in: PubMed
    73. Reynolds JE, Yang T, Qian L, Jenkinson JD, Zhou P, Eastman A, Craig RW. Mcl-1, a member of the Bcl-2 family, delays apoptosis induced by c-Myc overexpression in Chinese hamster ovary cells. Cancer Res. 1994 Dec 15; 54(24):6348-52. PMID: 7987827.
      View in: PubMed
    74. Ménétret JF, Craig R. Unfixed cryosections of striated muscle to study dynamic molecular events. Biophys J. 1994 Oct; 67(4):1612-9. PMID: 7819493.
      View in: PubMed
    75. Lehman W, Craig R, Vibert P. Ca(2+)-induced tropomyosin movement in Limulus thin filaments revealed by three-dimensional reconstruction. Nature. 1994 Mar 3; 368(6466):65-7. PMID: 8107884.
      View in: PubMed
    76. Lu L, Yang T, Markakis D, Guggino WB, Craig RW. Alterations in a voltage-gated K+ current during the differentiation of ML-1 human myeloblastic leukemia cells. J Membr Biol. 1993 Mar; 132(3):267-74. PMID: 8492309.
      View in: PubMed
    77. Craig R, Alamo L, Padrón R. Structure of the myosin filaments of relaxed and rigor vertebrate striated muscle studied by rapid freezing electron microscopy. J Mol Biol. 1992 Nov 20; 228(2):474-87. PMID: 1453458.
      View in: PubMed
    78. Frado LY, Craig R. Structural changes induced in scallop heavy meromyosin molecules by Ca2+ and ATP. J Muscle Res Cell Motil. 1992 Aug; 13(4):436-46. PMID: 1401039.
      View in: PubMed
    79. Frado LL, Craig R. Electron microscopy of the actin-myosin head complex in the presence of ATP. J Mol Biol. 1992 Jan 20; 223(2):391-7. PMID: 1738154.
      View in: PubMed
    80. Craig R, Padrón R, Alamo L. Direct determination of myosin filament symmetry in scallop striated adductor muscle by rapid freezing and freeze substitution. J Mol Biol. 1991 Jul 5; 220(1):125-32. PMID: 2067011.
      View in: PubMed
    81. Moody C, Lehman W, Craig R. Caldesmon and the structure of smooth muscle thin filaments: electron microscopy of isolated thin filaments. J Muscle Res Cell Motil. 1990 Apr; 11(2):176-85. PMID: 2351755.
      View in: PubMed
    82. Lehman W, Moody C, Craig R. Caldesmon and the structure of vertebrate smooth muscle thin filaments. A minireview. Ann N Y Acad Sci. 1990; 599:75-84. PMID: 2221678.
      View in: PubMed
    83. Lu L, Zeitlin PL, Guggino WB, Craig RW. Gene transfer by lipofection in rabbit and human secretory epithelial cells. Pflugers Arch. 1989 Nov; 415(2):198-203. PMID: 2594476.
      View in: PubMed
    84. Frado LL, Craig R. Structural changes induced in Ca2+-regulated myosin filaments by Ca2+ and ATP. J Cell Biol. 1989 Aug; 109(2):529-38. PMID: 2760106.
      View in: PubMed
    85. Cooke PH, Fay FS, Craig R. Myosin filaments isolated from skinned amphibian smooth muscle cells are side-polar. J Muscle Res Cell Motil. 1989 Jun; 10(3):206-20. PMID: 2503537.
      View in: PubMed
    86. Lehman W, Craig R, Lui J, Moody C. Caldesmon and the structure of smooth muscle thin filaments: immunolocalization of caldesmon on thin filaments. J Muscle Res Cell Motil. 1989 Apr; 10(2):101-12. PMID: 2760189.
      View in: PubMed
    87. Craig R, Padrón R, Kendrick-Jones J. Structural changes accompanying phosphorylation of tarantula muscle myosin filaments. J Cell Biol. 1987 Sep; 105(3):1319-27. PMID: 2958483.
      View in: PubMed
    88. Cooke PH, Kargacin G, Craig R, Fogarty K, Fay FS. Molecular structure and organization of filaments in single, skinned smooth muscle cells. Prog Clin Biol Res. 1987; 245:1-25. PMID: 3317435.
      View in: PubMed
    89. Cohen C, Vibert PJ, Craig RW, Phillips GN. Protein switches in muscle contraction. Prog Clin Biol Res. 1980; 40:209-31. PMID: 7005903.
      View in: PubMed
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    Craig's Networks
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