Ziploc-ing the structure: Triple helix formation is coordinated by rough endoplasmic reticulum resident PPIases

Biochimica et Biophysica Acta - General Subjects

Volumn 1850, Issue 10, 2015, Pages 1983-1993

  Ishikawa, Yoshihiro ^a,b   Boudko, Sergei ^a,b   Bächinger, Hans Peter ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b SHRINERS HOSPITAL FOR CHILDREN   (United States)

Author keywords

Collagen; Molecular chaperone; Peptidyl prolyl cis trans isomerase; Protein folding; Protein protein interaction; Rough endoplasmic reticulum

Indexed keywords

COLLAGEN; CYCLOPHILIN B; CYCLOPHILIN C; FK 506 BINDING PROTEIN; FK 506 BINDING PROTEIN 13; FK 506 BINDING PROTEIN 19; FK 506 BINDING PROTEIN 22; FK 506 BINDING PROTEIN 23; FK 506 BINDING PROTEIN 60; PEPTIDYLPROLYL ISOMERASE; UNCLASSIFIED DRUG;

CATALYSIS; COLLAGEN SYNTHESIS; COMPLEX FORMATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME REGULATION; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; HUMAN; INTRACELLULAR SIGNALING; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; REVIEW; ROUGH ENDOPLASMIC RETICULUM; TRIPLE HELIX; ANIMAL; BIOSYNTHESIS; ENDOPLASMIC RETICULUM; METABOLISM; PROTEIN SECONDARY STRUCTURE;

ANIMALS; COLLAGEN; ENDOPLASMIC RETICULUM; HUMANS; PEPTIDYLPROLYL ISOMERASE; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY;

EID: 84940575187     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.12.024     Document Type: Review

References (164)

1. C.J. Epstein, R.F. Goldberger, and C.B. Anfinsen The genetic control of tertiary protein structure: studies with model systems Cold Spring Harb. Symp. Quant. Biol. 28 1963 439 449
2. C.B. Anfinsen Principles that govern the folding of protein chains Science 181 1973 223 230
3. J.D. Bryngelson, J.N. Onuchic, N.D. Socci, and P.G. Wolynes Funnels, pathways, and the energy landscape of protein folding: a synthesis Proteins 21 1995 167 195
4. F.U. Hartl, A. Bracher, and M. Hayer-Hartl Molecular chaperones in protein folding and proteostasis Nature 475 2011 324 332
5. K. Liberek, A. Lewandowska, and S. Zietkiewicz Chaperones in control of protein disaggregation EMBO J. 27 2008 328 335
6. I. Braakman, and N.J. Bulleid Protein folding and modification in the mammalian endoplasmic reticulum Annu. Rev. Biochem. 80 2011 71 99
7. T. Gidalevitz, F. Stevens, and Y. Argon Orchestration of secretory protein folding by ER chaperones Biochim. Biophys. Acta, Mol. Cell Res. 1833 2013 2410 2424
8. G. Szabadkai, and R. Rizzuto Chaperones as parts of organelle networks P. Csermely, L. Vígh, Molecular Aspects of the Stress Response: Chaperones, Membranes and Networks vol. 594 2007 Springer New York 64 77
9. W. Voos Chaperone-protease networks in mitochondrial protein homeostasis Biochim. Biophys. Acta, Mol. Cell Res. 1833 2013 388 399
10. C.C. Trandinh, G.M. Pao, and M.H. Saier Jr. Structural and evolutionary relationships among the immunophilins: two ubiquitous families of peptidyl-prolyl cis-trans isomerases FASEB J. 6 1992 3410 3420
11. Q. Yao, M. Li, H. Yang, H. Chai, W. Fisher, and C. Chen Roles of cyclophilins in cancers and other organ systems World J. Surg. 29 2005 276 280
12. T. Anelli, and R. Sitia Protein quality control in the early secretory pathway EMBO J. 27 2008 315 327
13. Y. Ishikawa, and H.P. Bächinger A molecular ensemble in the rER for procollagen maturation Biochim. Biophys. Acta, Mol. Cell Res. 1833 2013 2479 2491
14. H.P. Bächinger, K. Mizuno, J. Vranka, and S. Boudko Collagen formation and structure L. Mander, H.-W. Liu, Comprehensive Natural Products II: Chemistry and Biology vol. Amino Acids, Peptides and Proteins 2010 Elsevier Ltd. 469 530
15. J.F. Bateman, R.P. Boot-Handford, and S.R. Lamande Genetic diseases of connective tissues: cellular and extracellular effects of ECM mutations Nat. Rev. Genet. 10 2009 173 183
16. J. Engel, and H. Bächinger Structure, stability and folding of the collagen triple helix J. Brinckmann, H. Notbohm, P.K. Müller, Collagen vol. 247 2005 Springer Berlin Heidelberg 7 33
17. S.P. Boudko, J. Engel, and H.P. Bächinger The crucial role of trimerization domains in collagen folding Int. J. Biochem. Cell Biol. 44 2012 21 32
18. A.V. Persikov, J.A.M. Ramshaw, A. Kirkpatrick, and B. Brodsky Amino acid propensities for the collagen triple-helix Biochemistry 39 2000 14960 14967
19. E. Pokidysheva, K.D. Zientek, Y. Ishikawa, K. Mizuno, J.A. Vranka, N.T. Montgomery, D.R. Keene, T. Kawaguchi, K. Okuyama, and H.P. Bächinger Posttranslational modifications in type I collagen from different tissues extracted from wild type and prolyl 3-hydroxylase 1 null mice J. Biol. Chem. 288 2013 24742 24752
20. D.M. Hudson, and D.R. Eyre Collagen prolyl 3-hydroxylation: a major role for a minor post-translational modification? Connect. Tissue Res. 54 2013 245 251
21. H.P. Bächinger, P. Bruckner, R. Timpl, D.J. Prockop, and J. Engel Folding mechanism of the triple helix in type-III collagen and type-III pN-collagen. Role of disulfide bridges and peptide bond isomerization Eur. J. Biochem. 106 1980 619 632
22. H.P. Bächinger, P. Bruckner, R. Timpl, and J. Engel The role of cis-trans isomerization of peptide bonds in the coil leads to and comes from triple helix conversion of collagen Eur. J. Biochem. 90 1978 605 613
23. P. Bruckner, and E.F. Eikenberry Formation of the triple helix of type I procollagen in cellulo. Temperature-dependent kinetics support a model based on cis in equilibrium trans isomerization of peptide bonds Eur. J. Biochem. 140 1984 391 395
24. H.P. Bächinger The influence of peptidyl-prolyl cis-trans isomerase on the in vitro folding of type III collagen J. Biol. Chem. 262 1987 17144 17148
25. B. Steinmann, P. Bruckner, and A. Superti-Furga Cyclosporin A slows collagen triple-helix formation in vivo: indirect evidence for a physiologic role of peptidyl-prolyl cis-trans-isomerase J. Biol. Chem. 266 1991 1299 1303
26. H.P. Bächinger, N.P. Morris, and J.M. Davis Thermal stability and folding of the collagen triple helix and the effects of mutations in osteogenesis imperfecta on the triple helix of type I collagen Am. J. Med. Genet. 45 1993 152 162
27. Y. Ishikawa, J.A. Vranka, S.P. Boudko, E. Pokidysheva, K. Mizuno, K. Zientek, D.R. Keene, A.M. Rashmir-Raven, K. Nagata, N.J. Winand, and H.P. Bächinger Mutation in cyclophilin B that causes hyperelastosis cutis in American quarter horse does not affect peptidylprolyl cis-trans isomerase activity but shows altered cyclophilin B-protein interactions and affects collagen folding J. Biol. Chem. 287 2012 22253 22265
28. Y. Ishikawa, J. Vranka, J. Wirz, K. Nagata, and H.P. Bächinger The rough endoplasmic reticulum-resident FK506-binding protein fkbp65 is a molecular chaperone that interacts with collagens J. Biol. Chem. 283 2008 31584 31590
29. Y. Ishikawa, and H.P. Bächinger A substrate preference for the rough endoplasmic reticulum resident protein FKBP22 during collagen biosynthesis J. Biol. Chem. 289 2014 18189 18201
30. S.R. Lamande, and J.F. Bateman Procollagen folding and assembly: the role of endoplasmic reticulum enzymes and molecular chaperones Semin. Cell Dev. Biol. 10 1999 455 464
31. T. Koide, and K. Nagata Collagen Biosynthesis J. Brinckmann, H. Notbohm, P.K. Müller, Collagen vol. 247 2005 Springer Berlin Heidelberg 85 114
32. E. Makareeva, N.A. Aviles, and S. Leikin Chaperoning osteogenesis: new protein-folding disease paradigms Trends Cell Biol. 21 2011 168 176
33. P.H. Byers, and W.G. Cole Osteogenesis imperfecta P.M. Royce, B. Stinmann, Connective Tissue and Heritable Disorders Second edition 2002 Wiley-Liss New York 285 430
34. F. Rauch, and F.H. Glorieux Osteogenesis imperfecta Lancet 363 2004 1377 1385
35. D. Eyre, and M. Weis Bone collagen: new clues to its mineralization mechanism from recessive osteogenesis imperfecta Calcif. Tissue Int. 93 2013 338 347
36. E.R. Valadares, T.B. Carneiro, P.M. Santos, A.C. Oliveira, and B. Zabel What is new in genetics and osteogenesis imperfecta classification? J. Pediatr 90 2014 536 541
37. F.S. van Dijk, I.M. Nesbitt, E.H. Zwikstra, P.G.J. Nikkels, S.R. Piersma, S.A. Fratantoni, C.R. Jimenez, M. Huizer, A.C. Morsman, J.M. Cobben, M.H.H. van Roij, M.W. Elting, J.I.M.L. Verbeke, L.C.D. Wijnaendts, N.J. Shaw, W. Högler, C. McKeown, E.A. Sistermans, A. Dalton, H. Meijers-Heijboer, and G. Pals PPIB mutations cause severe osteogenesis imperfecta Am. J. Human Genet. 85 2009 521 527
38. A.M. Barnes, E.M. Carter, W.A. Cabral, M. Weis, W. Chang, E. Makareeva, S. Leikin, C.N. Rotimi, D.R. Eyre, C.L. Raggio, and J.C. Marini Lack of cyclophilin B in osteogenesis imperfecta with normal collagen folding N. Engl. J. Med. 362 2010 521 528
39. S.M. Pyott, U. Schwarze, H.E. Christiansen, M.G. Pepin, D.F. Leistritz, R. Dineen, C. Harris, B.K. Burton, B. Angle, K. Kim, M.D. Sussman, M. Weis, D.R. Eyre, D.W. Russell, K.J. McCarthy, R.D. Steiner, and P.H. Byers Mutations in PPIB (cyclophilin B) delay type I procollagen chain association and result in perinatal lethal to moderate osteogenesis imperfecta phenotypes Hum. Mol. Genet. 20 2011 1595 1609
40. B.P. Kelley, F. Malfait, L. Bonafe, D. Baldridge, E. Homan, S. Symoens, A. Willaert, N. Elcioglu, L. Van Maldergem, C. Verellen-Dumoulin, Y. Gillerot, D. Napierala, D. Krakow, P. Beighton, A. Superti-Furga, A. De Paepe, and B. Lee Mutations in FKBP10 cause recessive osteogenesis imperfecta and bruck syndrome J. Bone Miner. Res. 26 2011 666 672
41. G. Venturi, E. Monti, L. Dalle Carbonare, M. Corradi, A. Gandini, M.T. Valenti, A. Boner, and F. Antoniazzi A novel splicing mutation in FKBP10 causing osteogenesis imperfecta with a possible mineralization defect Bone 50 2012 343 349
42. O. Steinlein, E. Aichinger, H. Trucks, and T. Sander Mutations in FKBP10 can cause a severe form of isolated osteogenesis imperfecta BMC Med. Genet. 12 2011 152
43. A.M. Barnes, W.A. Cabral, M. Weis, E. Makareeva, E.L. Mertz, S. Leikin, D. Eyre, C. Trujillo, and J.C. Marini Absence of FKBP10 in recessive type XI osteogenesis imperfecta leads to diminished collagen cross-linking and reduced collagen deposition in extracellular matrix Hum. Mutat. 33 2012 1589 1598
44. U. Schwarze, T. Cundy, S.M. Pyott, H.E. Christiansen, M.R. Hegde, R.A. Bank, G. Pals, A. Ankala, K. Conneely, L. Seaver, S.M. Yandow, E. Raney, D. Babovic-Vuksanovic, J. Stoler, Z. Ben-Neriah, R. Segel, S. Lieberman, L. Siderius, A. Al-Aqeel, M. Hannibal, L. Hudgins, E. McPherson, M. Clemens, M.D. Sussman, R.D. Steiner, J. Mahan, R. Smith, K. Anyane-Yeboa, J. Wynn, K. Chong, T. Uster, S. Aftimos, V.R. Sutton, E.C. Davis, L.S. Kim, M.A. Weis, D. Eyre, and P.H. Byers Mutations in FKBP10, which result in Bruck syndrome and recessive forms of osteogenesis imperfecta, inhibit the hydroxylation of telopeptide lysines in bone collagen Hum. Mol. Genet. 22 2013 1 17
45. R. Shaheen, M. Al-Owain, E. Faqeih, N. Al-Hashmi, A. Awaji, Z. Al-Zayed, and F.S. Alkuraya Mutations in FKBP10 cause both Bruck syndrome and isolated osteogenesis imperfecta in humans Am. J. Med. Genet. A 155 2011 1448 1452
46. E.D. Setijowati, F.S. van Dijk, J.M. Cobben, R.R. van Rijn, E.A. Sistermans, S.M.H. Faradz, S. Kawiyana, and G. Pals A novel homozygous 5 bp deletion in FKBP10 causes clinically Bruck syndrome in an Indonesian patient Eur. J. Med. Genet. 55 2012 17 21
47. P. Zhou, Y. Liu, F. Lv, M. Nie, Y. Jiang, O. Wang, W. Xia, X. Xing, and M. Li Novel mutations in FKBP10 and PLOD2 cause rare Bruck syndrome in Chinese patients PLoS ONE 9 2014 e107594
48. A.M. Barnes, G. Duncan, M. Weis, W. Paton, W.A. Cabral, E.L. Mertz, E. Makareeva, M.J. Gambello, F.L. Lacbawan, S. Leikin, A. Fertala, D.R. Eyre, S.J. Bale, and J.C. Marini Kuskokwim syndrome, a recessive congenital contracture disorder, extends the phenotype of FKBP10 mutations Hum. Mutat. 34 2013 1279 1288
49. M. Baumann, C. Giunta, B. Krabichler, F. Rüschendorf, N. Zoppi, M. Colombi, Reginald E. Bittner, S. Quijano-Roy, F. Muntoni, S. Cirak, G. Schreiber, Y. Zou, Y. Hu, Norma B. Romero, Robert Y. Carlier, A. Amberger, A. Deutschmann, V. Straub, M. Rohrbach, B. Steinmann, K. Rostásy, D. Karall, Carsten G. Bönnemann, J. Zschocke, and C. Fauth Mutations in FKBP14 cause a variant of Ehlers-Danlos syndrome with progressive kyphoscoliosis, myopathy, and hearing loss Am. J. Hum. Genet. 90 2012 201 216
50. P.H. Byers, and M.L. Murray Heritable collagen disorders: the paradigm of the Ehlers-Danlos syndrome J. Invest. Dermatol. 132 2012 E6 E11
51. F. Malfait, and A. De Paepe The Ehlers-Danlos syndrome J. Halper, Progress in Heritable Soft Connective Tissue Diseases vol. 802 2014 Springer Netherlands 129 143
52. M.J. Feige, S. Groscurth, M. Marcinowski, Y. Shimizu, H. Kessler, L.M. Hendershot, and J. Buchner An unfolded CH1 domain controls the assembly and secretion of IgG antibodies Mol. Cell 34 2009 569 579
53. G. Kozlov, S. Bastos-Aristizabal, P. Määttänen, A. Rosenauer, F. Zheng, A. Killikelly, J.-F. Trempe, D.Y. Thomas, and K. Gehring Structural basis of cyclophilin B binding by the calnexin/calreticulin P-domain J. Biol. Chem. 285 2010 35551 35557
54. P. Stocki, D.C. Chapman, L.A. Beach, and D.B. Williams Depletion of cyclophilins B and C Leads to dysregulation of endoplasmic reticulum redox homeostasis J. Biol. Chem. 289 2014 23086 23096
55. Y. Ishikawa, and H.P. Bächinger An additional function of the rough endoplasmic reticulum protein complex prolyl 3-hydroxylase 1 · cartilage-associated protein · cyclophilin B: the CXXXC Motif Reveals Disulfide Isomerase Activity In Vitro J. Biol. Chem. 288 2013 31437 31446
56. J. Kim, T.G. Choi, Y. Ding, Y. Kim, K.S. Ha, K.H. Lee, I. Kang, J. Ha, R.J. Kaufman, J. Lee, W. Choe, and S.S. Kim Overexpressed cyclophilin B suppresses apoptosis associated with ROS and Ca2 + homeostasis after ER stress J. Cell Sci. 121 2008 3636 3648
57. R. Bernasconi, T. Soldà, C. Galli, T. Pertel, J. Luban, and M. Molinari Cyclosporine A-sensitive, cyclophilin B-dependent endoplasmic reticulum-associated degradation PLoS ONE 5 2010 e13008
58. B. Schwanhausser, D. Busse, N. Li, G. Dittmar, J. Schuchhardt, J. Wolf, W. Chen, and M. Selbach Global quantification of mammalian gene expression control Nature 473 2011 337 342
59. J.R. Wisniewski, P. Ostasiewicz, K. Dus, D.F. Zielinska, F. Gnad, and M. Mann Extensive quantitative remodeling of the proteome between normal colon tissue and adenocarcinoma Mol. Syst. Biol. 8 2012 611
60. F.M. Boisvert, Y. Ahmad, M. Gierlinski, F. Charriere, D. Lamont, M. Scott, G. Barton, and A.I. Lamond A quantitative spatial proteomics analysis of proteome turnover in human cells Mol. Cell. Proteomics 11 2012 (M111 011429)
61. R. Morello, T.K. Bertin, Y. Chen, J. Hicks, L. Tonachini, M. Monticone, P. Castagnola, F. Rauch, F.H. Glorieux, J. Vranka, H.P. Bächinger, J.M. Pace, U. Schwarze, P.H. Byers, M. Weis, R.J. Fernandes, D.R. Eyre, Z. Yao, B.F. Boyce, and B. Lee CRTAP is required for prolyl 3-hydroxylation and mutations cause recessive osteogenesis imperfecta Cell 127 2006 291 304
62. E.R. Price, L.D. Zydowsky, M.J. Jin, C.H. Baker, F.D. McKeon, and C.T. Walsh Human cyclophilin B: a second cyclophilin gene encodes a peptidyl-prolyl isomerase with a signal sequence Proc. Natl. Acad. Sci. 88 1991 1903 1907
63. B. Zeng, J.R. MacDonald, J.G. Bann, K. Beck, J.E. Gambee, B.A. Boswell, and H.P. Bächinger Chicken FK506-binding protein, FKBP65, a member of the FKBP family of peptidylprolyl cis-trans isomerases, is only partially inhibited by FK506 Biochem. J. 330 1998 109 114
64. J.B. Nielsen, F. Foor, J.J. Siekierka, M.J. Hsu, N. Ramadan, N. Morin, A. Shafiee, A.M. Dahl, L. Brizuela, and G. Chrebet Yeast FKBP-13 is a membrane-associated FK506-binding protein encoded by the nonessential gene FKB2 Proc. Natl. Acad. Sci. 89 1992 7471 7475
65. Y. Ishikawa, J. Wirz, J.A. Vranka, K. Nagata, and H.P. Bächinger Biochemical characterization of the prolyl 3-hydroxylase 1 · cartilage-associated protein · cyclophilin B complex J. Biol. Chem. 284 2009 17641 17647
66. W.A. Cabral, I. Perdivara, M. Weis, M. Terajima, A.R. Blissett, W. Chang, J.E. Perosky, E.N. Makareeva, E.L. Mertz, S. Leikin, K.B. Tomer, K.M. Kozloff, D.R. Eyre, M. Yamauchi, and J.C. Marini Abnormal type I collagen post-translational modification and crosslinking in a cyclophilin B KO mouse model of recessive osteogenesis imperfecta PLoS Genet. 10 2014 e1004465
67. T. Smith, L.R. Ferreira, C. Hebert, K. Norris, and J.J. Sauk Hsp47 and cyclophilin B traverse the endoplasmic reticulum with procollagen into pre-Golgi intermediate vesicles: a role for Hsp47 and cyclophilin B in the export of procollagen from the endoplasmic reticulum J. Biol. Chem. 270 1995 18323 18328
68. J. Zhang, and H. Herscovitz Nascent lipidated apolipoprotein B is transported to the Golgi as an incompletely folded intermediate as probed by its association with network of endoplasmic reticulum molecular chaperones, GRP94, ERp72, BiP, calreticulin, and cyclophilin B J. Biol. Chem. 278 2003 7459 7468
69. T. Horibe, C. Yosho, S. Okada, M. Tsukamoto, H. Nagai, Y. Hagiwara, Y. Tujimoto, and M. Kikuchi The chaperone activity of protein disulfide isomerase is affected cyclophilin B and cyclosporin A in vitro J. Biochem. 132 2002 401 407
70. L. Meunier, Y.-K. Usherwood, K.T. Chung, and L.M. Hendershot A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins Mol. Biol. Cell 13 2002 4456 4469
71. G. Jansen, P. Määttänen, A.Y. Denisov, L. Scarffe, B. Schade, H. Balghi, K. Dejgaard, L.Y. Chen, W.J. Muller, K. Gehring, and D.Y. Thomas An interaction map of endoplasmic reticulum chaperones and foldases Mol. Cell. Proteomics 11 2012 710 723
72. J.A. Vranka, L.Y. Sakai, and H.P. Bächinger Prolyl 3-hydroxylase 1, enzyme characterization and identification of a novel family of enzymes J. Biol. Chem. 279 2004 23615 23621
73. A.M. Barnes, W. Chang, R. Morello, W.A. Cabral, M. Weis, D.R. Eyre, S. Leikin, E. Makareeva, N. Kuznetsova, T.E. Uveges, A. Ashok, A.W. Flor, J.J. Mulvihill, P.L. Wilson, U.T. Sundaram, B. Lee, and J.C. Marini Deficiency of cartilage-associated protein in recessive lethal osteogenesis imperfecta N. Engl. J. Med. 355 2006 2757 2764
74. W.A. Cabral, W. Chang, A.M. Barnes, M. Weis, M.A. Scott, S. Leikin, E. Makareeva, N.V. Kuznetsova, K.N. Rosenbaum, C.J. Tifft, D.I. Bulas, C. Kozma, P.A. Smith, D.R. Eyre, and J.C. Marini Prolyl 3-hydroxylase 1 deficiency causes a recessive metabolic bone disorder resembling lethal/severe osteogenesis imperfecta Nat. Genet. 39 2007 359 365
75. D. Baldridge, U. Schwarze, R. Morello, J. Lennington, T.K. Bertin, J.M. Pace, M.G. Pepin, M. Weis, D.R. Eyre, J. Walsh, D. Lambert, A. Green, H. Robinson, M. Michelson, G. Houge, C. Lindman, J. Martin, J. Ward, E. Lemyre, J.J. Mitchell, D. Krakow, D.L. Rimoin, D.H. Cohn, P.H. Byers, and B. Lee CRTAP and LEPRE1 mutations in recessive osteogenesis imperfecta Hum. Mutat. 29 2008 1435 1442
76. M. Takagi, T. Ishii, A.M. Barnes, M. Weis, N. Amano, M. Tanaka, R. Fukuzawa, G. Nishimura, D.R. Eyre, J.C. Marini, and T. Hasegawa A novel mutation in LEPRE1 that eliminates only the KDEL ER - retrieval sequence causes non-lethal osteogenesis imperfecta PLoS ONE 7 2012 e36809
77. K.I. Kivirikko, and R. Myllyla Posttranslational enzymes in the biosynthesis of collagen: intracellular enzymes Methods Enzymol. 82 Pt A 1982 245 304
78. M. Yamauchi, and M. Sricholpech Lysine post-translational modifications of collagen Essays Biochem. 52 2012 113 133
79. M. Yamauchi, and M. Shiiba Lysine hydroxylation and cross-linking of collagen C. Kannicht, Post-translational Modifications of Proteins vol. 446 2008 Humana Press 95 108
80. K. Takaluoma, M. Hyry, J. Lantto, R. Sormunen, R.A. Bank, K.I. Kivirikko, J. Myllyharju, and R. Soininen Tissue-specific changes in the hydroxylysine content and cross-links of collagens and alterations in fibril morphology in lysyl hydroxylase 1 knock-out mice J. Biol. Chem. 282 2007 6588 6596
81. D. Eyre, P. Shao, M. Ann Weis, and B. Steinmann The kyphoscoliotic type of Ehlers-Danlos syndrome (type VI): differential effects on the hydroxylation of lysine in collagens I and II revealed by analysis of cross-linked telopeptides from urine Mol. Genet. Metab. 76 2002 211 216
82. A.-M. Zuurmond, A.J. van der Slot-Verhoeven, E.A. van Dura, J. De Groot, and R.A. Bank Minoxidil exerts different inhibitory effects on gene expression of lysyl hydroxylase 1, 2, and 3: implications for collagen cross-linking and treatment of fibrosis Matrix Biol. 24 2005 261 270
83. M.J. Bottomley, M.R. Batten, R.A. Lumb, and N.J. Bulleid Quality control in the endoplasmic reticulum: PDI mediates the ER retention of unassembled procollagen C-propeptides Curr. Biol. 11 2001 1114 1118
84. S.R. Lamande, S.D. Chessler, S.B. Golub, P.H. Byers, D. Chan, W.G. Cole, D.O. Sillence, and J.F. Bateman Endoplasmic reticulum-mediated quality control of type I collagen production by cells from osteogenesis imperfecta patients with mutations in the pro alpha 1 (I) chain carboxyl-terminal propeptide which impair subunit assembly J. Biol. Chem. 270 1995 8642 8649
85. J.M. Pace, C.D. Kuslich, M.C. Willing, and P.H. Byers Disruption of one intra-chain disulphide bond in the carboxyl-terminal propeptide of the proalpha1(I) chain of type I procollagen permits slow assembly and secretion of overmodified, but stable procollagen trimers and results in mild osteogenesis imperfecta J. Med. Genet. 38 2001 443 449
86. R. Wilson, J.F. Lees, and N.J. Bulleid Protein disulfide isomerase acts as a molecular chaperone during the assembly of procollagen J. Biol. Chem. 273 1998 9637 9643
87. C.E. Patterson, T. Schaub, E.J. Coleman, and E.C. Davis Developmental regulation of FKBP65. An ER-localized extracellular matrix binding-protein Mol. Biol. Cell 11 2000 3925 3935
88. K.L.Y. Cheung, M. Bates, and V.S. Ananthanarayanan Effect of FKBP65, a putative elastin chaperone, on the coacervation of tropoelastin in vitro Biochem. Cell Biol. 88 2010 917 925
89. M. Miao, S.E. Reichheld, L.D. Muiznieks, Y. Huang, and F.W. Keeley Elastin binding protein and FKBP65 modulate in vitro self-assembly of human tropoelastin Biochemistry 52 2013 7731 7741
90. C.D. Lietman, A. Rajagopal, E.P. Homan, E. Munivez, M.-M. Jiang, T.K. Bertin, Y. Chen, J. Hicks, M. Weis, D. Eyre, B. Lee, and D. Krakow Connective tissue alterations in Fkbp10 -/- mice Hum. Mol. Genet. 23 2014 4822 4831
91. S.P. Boudko, Y. Ishikawa, J. Nix, M.S. Chapman, and H.P. Bächinger Structure of human peptidyl-prolyl cis-trans isomerase FKBP22 containing two EF-hand motifs Protein Sci. 23 2014 67 75
92. M.L. Murray, M. Yang, C. Fauth, and P.H. Byers FKBP14-related Ehlers-Danlos syndrome: expansion of the phenotype to include vascular complications Am. J. Med. Genet. A 164 2014 1750 1755
93. A.A. Aldeeri, A.M. Alazami, H. Hijazi, F. Alzahrani, and F.S. Alkuraya Excessively redundant umbilical skin as a potential early clinical feature of Morquio syndrome and FKBP14-related Ehlers-Danlos syndrome Clin. Genet. 86 2014 469 472
94. C. Budiman, K. Bando, C. Angkawidjaja, Y. Koga, K. Takano, and S. Kanaya Engineering of monomeric FK506-binding protein 22 with peptidyl prolyl cis-trans isomerase. Importance of a V-shaped dimeric structure for binding to protein substrate FEBS J. 276 2009 4091 4101
95. C. Budiman, C. Angkawidjaja, H. Motoike, Y. Koga, K. Takano, and S. Kanaya Crystal structure of N-domain of FKBP22 from Shewanella sp. SIB1: dimer dissociation by disruption of Val-Leu knot Protein Sci. 20 2011 1755 1764
96. S.K. Nigam, Y.J. Jin, M.J. Jin, K.T. Bush, B.E. Bierer, and S.J. Burakoff Localization of the FK506-binding protein, FKBP 13, to the lumen of the endoplasmic reticulum Biochem. J. 294 1993 511 515
97. J.A. Partaledis, and V. Berlin The FKB2 gene of Saccharomyces cerevisiae, encoding the immunosuppressant-binding protein FKBP-13, is regulated in response to accumulation of unfolded proteins in the endoplasmic reticulum Proc. Natl. Acad. Sci. 90 1993 5450 5454
98. K.T. Bush, B.A. Hendrickson, and S.K. Nigam Induction of the FK506-binding protein, FKBP13, under conditions which misfold proteins in the endoplasmic reticulum Biochem. J. 303 1994 705 708
99. H. Coe, and M. Michalak ERp57, a multifunctional endoplasmic reticulum resident oxidoreductase Int. J. Biochem. Cell Biol. 42 2010 796 799
100. S. Rulten, R. Kinloch, H. Tateossian, C. Robinson, L. Gettins, and J. Kay The human FK506-binding proteins: characterization of human FKBP19 Mamm. Genome 17 2006 322 331
101. N. Hanagata, X. Li, H. Morita, T. Takemura, J. Li, and T. Minowa Characterization of the osteoblast-specific transmembrane protein IFITM5 and analysis of IFITM5-deficient mice J. Bone Miner. Metab. 29 2011 279 290
102. N. Hanagata, and X. Li Osteoblast-enriched membrane protein IFITM5 regulates the association of CD9 with an FKBP11-CD81-FPRP complex and stimulates expression of interferon-induced genes Biochem. Biophys. Res. Commun. 409 2011 378 384
103. T. Tsukamoto, X. Li, H. Morita, T. Minowa, T. Aizawa, N. Hanagata, and M. Demura Role of S-palmitoylation on IFITM5 for the interaction with FKBP11 in osteoblast cells PLoS ONE 8 2013 e75831
104. T.-J. Cho, K.-E. Lee, S.-K. Lee, Su. J. Song, Kyung J. Kim, D. Jeon, G. Lee, H.-N. Kim, Hye R. Lee, H.-H. Eom, Zang H. Lee, O.-H. Kim, W.-Y. Park, Sung S. Park, S. Ikegawa, and Won J. Yoo H. Choi, J.-W. Kim, A single recurrent mutation in the 5′-UTR of IFITM5 causes osteogenesis imperfecta type V Am. J. Human Genet. 91 2012 343 348
105. O. Semler, L. Garbes, K. Keupp, D. Swan, K. Zimmermann, J. Becker, S. Iden, B. Wirth, P. Eysel, F. Koerber, E. Schoenau, Stefan K. Bohlander, B. Wollnik, and C. Netzer A mutation in the 5′-UTR of IFITM5 creates an in-frame start codon and causes autosomal-dominant osteogenesis imperfecta type V with hyperplastic callus Am. J. Human Genet. 91 2012 349 357
106. F. Rauch, P. Moffatt, M. Cheung, P. Roughley, L. Lalic, A.M. Lund, N. Ramirez, S. Fahiminiya, J. Majewski, and F.H. Glorieux Osteogenesis imperfecta type V: marked phenotypic variability despite the presence of the IFITM5 c.-14C > T mutation in all patients J. Med. Genet. 50 2013 21 24
107. H. Hoyer-Kuhn, O. Semler, L. Garbes, K. Zimmermann, J. Becker, B. Wollnik, E. Schoenau, and C. Netzer A nonclassical IFITM5 mutation located in the coding region causes severe osteogenesis imperfecta with prenatal onset J. Bone Miner. Res. 29 2014 1387 1391
108. C.R. Farber, A. Reich, A.M. Barnes, P. Becerra, F. Rauch, W.A. Cabral, A. Bae, A. Quinlan, F.H. Glorieux, T.L. Clemens, and J.C. Marini A novel IFITM5 mutation in severe atypical osteogenesis imperfecta type VI impairs osteoblast production of pigment epithelium-derived factor J. Bone Miner. Res. 29 2014 1402 1411
109. M. Feng, C. Gu, S. Ma, Y. Wang, H. Liu, R. Han, J. Gao, Y. Long, and H. Mi Mouse FKBP23 mediates conformer-specific functions of BiP by catalyzing Pro117 cis/trans isomerization Biochem. Biophys. Res. Commun. 408 2011 537 540
110. X. Zhang, Y. Wang, H. Li, W. Zhang, D. Wu, and H. Mi The mouse FKBP23 binds to BiP in ER and the binding of C-terminal domain is interrelated with Ca2 + concentration FEBS Lett. 559 2004 57 60
111. T. Pozzan, R. Rizzuto, P. Volpe, and J. Meldolesi Molecular and Cellular Physiology of Intracellular Calcium Stores 1994
112. Y. Wang, R. Han, D. Wu, J. Li, C. Chen, H. Ma, and H. Mi The binding of FKBP23 to BiP modulates BiP's ATPase activity with its PPIase activity Biochem. Biophys. Res. Commun. 354 2007 315 320
113. K. Fukuda, Y. Tanigawa, G. Fujii, S. Yasugi, and S. Hirohashi cFKBP/SMAP; a novel molecule involved in the regulation of smooth muscle differentiation Development 125 1998 3535 3542
114. M. Shadidy, X. Caubit, R. Olsen, O.M. Seternes, U. Moens, and S. Krauss Biochemical analysis of mouse FKBP60, a novel member of the FKPB family Biochim. Biophys. Acta Gene Struct. Expr. 1446 1999 295 307
115. J. Donggyu, L. MyungSoo, C. Eun-Gyung, P. Dongeun, A.K. Christine, and K. MoonGyo Identification and genetic mapping of the mouse Fkbp9 gene encoding a new member of FK506-binding protein family Mol. Cells 12 2001 272 275
116. H. Schneider, N. Charara, R. Schmitz, S. Wehrli, V. Mikol, M.G.M. Zurini, V.F.J. Quesniaux, and N.R. Movva Human cyclophilin C: primary structure, tissue distribution, and determination of binding specificity for cyclosporins Biochemistry 33 1994 8218 8224
117. H. Ke, Y. Zhao, F. Luo, I. Weissman, and J. Friedman Crystal structure of murine cyclophilin C complexed with immunosuppressive drug cyclosporin A Proc. Natl. Acad. Sci. 90 1993 11850 11854
118. J. Friedman, and I. Weissman Two cytoplasmic candidates for immunophilin action are revealed by affinity for a new cyclophilin: one in the presence and one in the absence of CsA Cell 66 1991 799 806
119. R.J. Bram, D.T. Hung, P.K. Martin, S.L. Schreiber, and G.R. Crabtree Identification of the immunophilins capable of mediating inhibition of signal transduction by cyclosporin A and FK506: roles of calcineurin binding and cellular location Mol. Cell. Biol. 13 1993 4760 4769
120. M. Trahey, and I.L. Weissman Cyclophilin C-associated protein: A normal secreted glycoprotein that down-modulates endotoxin and proinflammatory responses in vivo Proc. Natl. Acad. Sci. 96 1999 3006 3011
121. T.L. Davis, J.R. Walker, V. Campagna-Slater, P.J. Finerty Jr., R. Paramanathan, G. Bernstein, F. MacKenzie, W. Tempel, H. Ouyang, W.H. Lee, E.Z. Eisenmesser, and S. Dhe-Paganon Structural and biochemical characterization of the human cyclophilin family of peptidyl-prolyl isomerases PLoS Biol. 8 2010 e1000439
122. E.Z. Eisenmesser, D.A. Bosco, M. Akke, and D. Kern Enzyme dynamics during catalysis Science 295 2002 1520 1523
123. L.W. Schultz, P.K. Martin, J. Liang, S.L. Schreiber, and J. Clardy Atomic structure of the immunophilin FKBP13-FK506 complex: insights into the composite binding surface for calcineurin J. Am. Chem. Soc. 116 1994 3129 3130
124. G.D. Van Duyne, R.F. Standaert, P.A. Karplus, S.L. Schreiber, and J. Clardy Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin J. Mol. Biol. 229 1993 105 124
125. E. Krissinel, and K. Henrick Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallogr. D 60 2004 2256 2268
126. M.T. DeCenzo, S.T. Park, B.P. Jarrett, R.A. Aldape, O. Futer, M.A. Murcko, and D.J. Livingston FK506-binding protein mutational analysis: defining the active-site residue contributions to catalysis and the stability of ligand complexes Protein Eng. 9 1996 173 180
127. C. Drögemüller, D. Becker, A. Brunner, B. Haase, P. Kircher, F. Seeliger, M. Fehr, U. Baumann, K. Lindblad-Toh, and T. Leeb A missense mutation in the SERPINH1 gene in dachshunds with osteogenesis imperfecta PLoS Genet. 5 2009 e1000579
128. H.E. Christiansen, U. Schwarze, S.M. Pyott, A. AlSwaid, M. Al Balwi, S. Alrasheed, M.G. Pepin, M.A. Weis, D.R. Eyre, and P.H. Byers Homozygosity for a missense mutation in SERPINH1, which encodes the collagen chaperone protein HSP47, results in severe recessive osteogenesis imperfecta Am. J. Hum. Genet. 86 2010 389 398
129. P. Lapunzina, M. Aglan, S. Temtamy, J.A. Caparrós-Martín, M. Valencia, R. Letón, V. Martínez-Glez, R. Elhossini, K. Amr, N. Vilaboa, and V.L. Ruiz-Perez Identification of a frameshift mutation in osterix in a patient with recessive osteogenesis imperfecta Am. J. Hum. Genet. 87 2010 110 114
130. J. Becker, O. Semler, C. Gilissen, Y. Li, Hanno J. Bolz, C. Giunta, C. Bergmann, M. Rohrbach, F. Koerber, K. Zimmermann, P. de Vries, B. Wirth, E. Schoenau, B. Wollnik, Joris A. Veltman, A. Hoischen, and C. Netzer Exome sequencing identifies truncating mutations in human SERPINF1 in autosomal-recessive osteogenesis imperfecta Am. J. Hum. Genet. 88 2011 362 371
131. G. Venturi, A. Gandini, E. Monti, L.D. Carbonare, M. Corradi, M. Vincenzi, M.T. Valenti, M. Valli, E. Pelilli, A. Boner, M. Mottes, and F. Antoniazzi Lack of expression of SERPINF1, the gene coding for pigment epithelium-derived factor, causes progressively deforming osteogenesis imperfecta with normal type I collagen J. Bone Miner. Res. 27 2012 723 728
132. S.Y. Cho, C.-S. Ki, Y.B. Sohn, S.J. Kim, S.H. Maeng, and D.-K. Jin Osteogenesis imperfecta type VI with severe bony deformities caused by novel compound heterozygous mutations in SERPINF1 J. Korean Med. Sci. 28 2013 1107 1110
133. R. Shaheen, A.M. Alazami, M.J. Alshammari, E. Faqeih, N. Alhashmi, N. Mousa, A. Alsinani, S. Ansari, F. Alzahrani, M. Al-Owain, Z.S. Alzayed, and F.S. Alkuraya Study of autosomal recessive osteogenesis imperfecta in Arabia reveals a novel locus defined by TMEM38B mutation J. Med. Genet. 49 2012 630 635
134. M. Volodarsky, B. Markus, I. Cohen, O. Staretz-Chacham, H. Flusser, D. Landau, I. Shelef, Y. Langer, and O.S. Birk A deletion mutation in TMEM38B associated with autosomal recessive osteogenesis imperfecta Hum. Mutat. 34 2013 582 586
135. E. Rubinato, A. Morgan, A. D'Eustacchio, V. Pecile, G. Gortani, P. Gasparini, and F. Faletra A novel deletion mutation involving TMEM38B in a patient with autosomal recessive osteogenesis imperfecta Gene 545 2014 290 292
136. V. Martínez-Glez, M. Valencia, J.A. Caparrós-Martín, M. Aglan, S. Temtamy, J. Tenorio, V. Pulido, U. Lindert, M. Rohrbach, D. Eyre, C. Giunta, P. Lapunzina, and V.L. Ruiz-Perez Identification of a mutation causing deficient BMP1/mTLD proteolytic activity in autosomal recessive osteogenesis imperfecta Hum. Mutat. 33 2012 343 350
137. M. Valencia, J.A. Caparrós-Martin, M.S. Sirerol-Piquer, J.M. García-Verdugo, V. Martínez-Glez, P. Lapunzina, S. Temtamy, M. Aglan, A.M. Lund, P.G.J. Nikkels, V.L. Ruiz-Perez, and E. Ostergaard Report of a newly indentified patient with mutations in BMP1 and underlying pathogenetic aspects Am. J. Med. Genet. A 164 2014 1143 1150
138. S. Fahiminiya, J. Majewski, J. Mort, P. Moffatt, F.H. Glorieux, and F. Rauch Mutations in WNT1 are a cause of osteogenesis imperfecta J. Med. Genet. 50 2013 345 348
139. Shawna M. Pyott, Thao T. Tran, Dru F. Leistritz, Melanie G. Pepin, Nancy J. Mendelsohn, Renee T. Temme, Bridget A. Fernandez, Solaf M. Elsayed, E. Elsobky, I. Verma, S. Nair, Emily H. Turner, Joshua D. Smith, Gail P. Jarvik, and Peter H. Byers WNT1 mutations in families affected by moderately severe and progressive recessive osteogenesis imperfecta Am. J. Hum. Genet. 92 2013 590 597
140. C.M. Laine, K.S. Joeng, P.M. Campeau, R. Kiviranta, K. Tarkkonen, M. Grover, J.T. Lu, M. Pekkinen, M. Wessman, T.J. Heino, V. Nieminen-Pihala, M. Aronen, T. Laine, H. Kröger, W.G. Cole, A.-E. Lehesjoki, L. Nevarez, D. Krakow, C.J.R. Curry, D.H. Cohn, R.A. Gibbs, B.H. Lee, and O. Mäkitie WNT1 mutations in early-onset osteoporosis and osteogenesis imperfecta N. Engl. J. Med. 368 2013 1809 1816
141. S. Symoens, F. Malfait, S. D'hondt, B. Callewaert, A. Dheedene, W. Steyaert, H. Bächinger, A. De Paepe, H. Kayserili, and P. Coucke Deficiency for the ER-stress transducer OASIS causes severe recessive osteogenesis imperfecta in humans Orphanet J. Rare Dis. 8 2013 154
142. J.A. Vranka, E. Pokidysheva, L. Hayashi, K. Zientek, K. Mizuno, Y. Ishikawa, K. Maddox, S. Tufa, D.R. Keene, R. Klein, and H.P. Bächinger Prolyl 3-hydroxylase 1 null mice display abnormalities in fibrillar collagen-rich tissues such as tendons, skin, and bones J. Biol. Chem. 285 2010 17253 17262
143. T.A. Knappe, B. Eckert, P. Schaarschmidt, C. Scholz, and F.X. Schmid Insertion of a chaperone domain converts FKBP12 into a powerful catalyst of protein folding J. Mol. Biol. 368 2007 1458 1468
144. R.P. Jakob, G. Zoldák, T. Aumüller, and F.X. Schmid Chaperone domains convert prolyl isomerases into generic catalysts of protein folding Proc. Natl. Acad. Sci. 106 2009 20282 20287
145. A.-J. Geitner, and F.X. Schmid Combination of the human prolyl isomerase FKBP12 with unrelated chaperone domains leads to chimeric folding enzymes with high activity J. Mol. Biol. 420 2012 335 349
146. A.-J. Geitner, E. Varga, M. Wehmer, and F.X. Schmid Generation of a highly active folding enzyme by combining a parvulin-type prolyl isomerase from SurA with an unrelated chaperone domain J. Mol. Biol. 425 2013 4089 4098
147. T. Horibe, C. Yosho, S. Okada, M. Tsukamoto, H. Nagai, Y. Hagiwara, Y. Tujimoto, and M. Kikuchi The chaperone activity of protein disulfide isomerase is affected by cyclophilin B and cyclosporin A in vitro J. Biochem. 132 2002 401 407
148. Y. Ishida, and K. Nagata Hsp47 as a collagen-specific molecular chaperone Methods Enzymol. 499 2011 167 182
149. J.W. Choi, S.L. Sutor, L. Lindquist, G.L. Evans, B.J. Madden, H.R. Bergen III, T.E. Hefferan, M.J. Yaszemski, and R.J. Bram Severe osteogenesis imperfecta in cyclophilin B-deficient mice PLoS Genet. 5 2009 e1000750
150. W. Chang, A.M. Barnes, W.A. Cabral, J.N. Bodurtha, and J.C. Marini Prolyl 3-hydroxylase 1 and CRTAP are mutually stabilizing in the endoplasmic reticulum collagen prolyl 3-hydroxylation complex Hum. Mol. Genet. 19 2010 223 234
151. I.M.B. Amor, F. Rauch, K. Gruenwald, M. Weis, D.R. Eyre, P. Roughley, F.H. Glorieux, and R. Morello Severe osteogenesis imperfecta caused by a small in-frame deletion in CRTAP Am. J. Med. Genet. A 155 2011 2865 2870
152. I. Grafe, T. Yang, S. Alexander, E.P. Homan, C. Lietman, M.M. Jiang, T. Bertin, E. Munivez, Y. Chen, B. Dawson, Y. Ishikawa, M.A. Weis, T.K. Sampath, C. Ambrose, D. Eyre, H.P. Bächinger, and B. Lee Excessive transforming growth factor-[beta] signaling is a common mechanism in osteogenesis imperfecta Nat. Med. 20 2014 670 675
153. S. Kalamajski, and A. Oldberg The role of small leucine-rich proteoglycans in collagen fibrillogenesis Matrix Biol. 29 2010 248 253
154. K. Saito, M. Chen, F. Bard, S. Chen, H. Zhou, D. Woodley, R. Polischuk, R. Schekman, and V. Malhotra TANGO1 facilitates cargo loading at endoplasmic reticulum exit sites Cell 136 2009 891 902
155. D.G. Wilson, K. Phamluong, L. Li, M. Sun, T.C. Cao, P.S. Liu, Z. Modrusan, W.N. Sandoval, L. Rangell, R.A.D. Carano, A.S. Peterson, and M.J. Solloway Global defects in collagen secretion in a Mia3/TANGO1 knockout mouse J. Cell Biol. 193 2011 935 951
156. K. Saito, K. Yamashiro, Y. Ichikawa, P. Erlmann, K. Kontani, V. Malhotra, and T. Katada cTAGE5 mediates collagen secretion through interaction with TANGO1 at endoplasmic reticulum exit sites Mol. Biol. Cell 22 2011 2301 2308
157. K. Saito, K. Yamashiro, N. Shimazu, T. Tanabe, K. Kontani, and T. Katada Concentration of Sec12 at ER exit sites via interaction with cTAGE5 is required for collagen export J. Cell Biol. 206 2014 751 762
158. V. Malhotra, and P. Erlmann Protein Export at the ER: Loading Big Collagens Into COPII Carriers 2011
159. J.J. Siekierka, S.H.Y. Hung, M. Poe, C.S. Lin, and N.H. Sigal A cytosolic binding protein for the immunosuppressant FK506 has peptidyl-prolyl isomerase activity but is distinct from cyclophilin Nature 341 1989 755 757
160. T. Jayaraman, A.M. Brillantes, A.P. Timerman, S. Fleischer, H. Erdjument-Bromage, P. Tempst, and A.R. Marks FK506 binding protein associated with the calcium release channel (ryanodine receptor) J. Biol. Chem. 267 1992 9474 9477
161. C. Hidalgo Cross talk between Ca2 + and redox signalling cascades in muscle and neurons through the combined activation of ryanodine receptors/Ca2 + release channels Philos. Trans. R. Soc. Biol. Sci. 360 2005 2237 2246
162. D. MacMillan FK506 binding proteins: cellular regulators of intracellular Ca2 + signalling Eur. J. Pharmacol. 700 2013 181 193
163. S. McNicholas, E. Potterton, K.S. Wilson, and M.E. Noble Presenting your structures: the CCP4mg molecular-graphics software Acta Crystallogr. D Biol. Crystallogr. 67 2011 386 394
164. Y. Zhao, and H. Ke Mechanistic implication of crystal structures of the cyclophilin-dipeptide complexes Biochemistry 35 1996 7362 7368