Gain of glycosylation in integrin α3 causes lung disease and nephrotic syndrome

Journal of Clinical Investigation

Volumn 122, Issue 12, 2012, Pages 4375-4387

  Nicolaou, Nayia ^a   Margadant, Coert ^b   Kevelam, Sietske H ^a   Lilien, Marc R ^c   Oosterveld, Michiel J S ^c   Kreft, Maaike ^b   Van Eerde, Albertien M ^a   Pfundt, Rolph ^d   Terhal, Paulien A ^a   Van Der Zwaag, Bert ^a   Nikkels, Peter G J ^a   Sachs, Norman ^b   Goldschmeding, Roel ^a   Knoers, Nine V A M ^a   Renkema, Kirsten Y ^a   Sonnenberg, Arnoud ^b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ALPHA3 INTEGRIN; BETA1 INTEGRIN; CD151 ANTIGEN; PROTEASOME; SERINE; UBIQUITIN; VERY LATE ACTIVATION ANTIGEN 3;

AMINO ACID SUBSTITUTION; ARTICLE; CASE REPORT; CONGENITAL NEPHROTIC SYNDROME; DIMERIZATION; ENDOPLASMIC RETICULUM; FATALITY; FEMALE; GAIN OF FUNCTION MUTATION; GENE EXPRESSION; HOMOZYGOSITY; HUMAN; INTERSTITIAL LUNG DISEASE; MISSENSE MUTATION; MULTIPLE ORGAN FAILURE; PODOCYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION;

ANTIGENS, CD151; ANTIGENS, CD29; BASE SEQUENCE; CELLS, CULTURED; ENDOPLASMIC RETICULUM; FATAL OUTCOME; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION STUDIES; GLOMERULAR MESANGIUM; GLYCOSYLATION; HUMANS; INFANT; INTEGRIN ALPHA3; LUNG DISEASES, INTERSTITIAL; MODELS, MOLECULAR; NEPHROTIC SYNDROME; PEDIGREE; PODOCYTES; POINT MUTATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN MULTIMERIZATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; SEQUENCE ANALYSIS, DNA;

EID: 84870522502     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI64100     Document Type: Article

References (54)

1. Campbell ID, Humphries MJ. Integrin structure, activation, and interactions. Cold Spring Harb Perspect Biol. 2011;3(3):pii:a004994.
2. Geiger B, Yamada KM. Molecular architecture and function of matrix adhesions. Cold Spring Harb Perspect Biol. 2011;3(5):pii:a005033.
3. Kim C, Ye F, Ginsberg MH. Regulation of integrin activation. Annu Rev Cell Dev Biol. 2011;27:321-345.
4. Caswell PT, Vadrevu S, Norman JC. Integrins: masters and slaves of endocytic transport. Nat Rev Mol Cell Biol. 2009;10(12):843-853.
5. Margadant C, Monsuur HN, Norman JC, Sonnenberg A. Mechanisms of integrin activation and trafficking. Curr Opin Cell Biol. 2011;23(5):607-614.
6. Lissitzky JC, et al. Endoproteolytic processing of integrin pro-alpha subunits involves the redundant function of furin and proprotein convertase (PC) 5A, but not paired basic amino acid converting enzyme (PACE) 4, PC5B or PC7. Biochem J. 2000;346:133-138.
7. Delwel GO, Kuikman I, van der Schors RC, de Melker AA, Sonnenberg A. Identification of the cleavage sites in the alpha6A integrin subunit: structural requirements for cleavage and functional analysis of the uncleaved alpha6Abeta1 integrin. Biochem J. 1997;324:263-272. (Pubitemid 27229392)
8. Pulkkinen L, Uitto J. Mutation analysis and molecular genetics of epidermolysis bullosa. Matrix Biol. 1999;18(1):29-42. (Pubitemid 29213825)
9. Nurden AT, Fiore M, Nurden P, Pillois X. Glanzmann thrombasthenia: a review of ITGA2B and ITGB3 defects with emphasis on variants, phenotypic variability, and mouse models. Blood. 2011;118(23):5996-6005.
10. Hayashi YK, et al. Mutations in the integrin alpha7 gene cause congenital myopathy. Nat Genet. 1998;19(1):94-97. (Pubitemid 28242033)
11. Hogg N, Patzak I, Willenbrock F. The insider's guide to leukocyte integrin signalling and function. Nat Rev Immunol. 2011;11(6):416-426.
12. Wickström SA, Radovanac K, Fässler R. Genetic analyses of integrin signaling. Cold Spring Harb Perspect Biol. 2011;3(2):pii:a005116.
13. Kreidberg JA, et al. Alpha3beta1 integrin has a crucial role in kidney and lung organogenesis. Development. 1996;122(11):3537-3547. (Pubitemid 26395995)
14. DiPersio CM, Hodivala-Dilke KM, Jaenisch R, Kreidberg JA, Hynes RO. alpha3beta1 integrin is required for normal development of the epidermal basement membrane. J Cell Biol. 1997;137(3):729-742. (Pubitemid 27200673)
15. Hodivala-Dilke KM, DiPersio CM, Kreidberg JA, Hynes RO. Novel roles for alpha3beta1 integrin as a regulator of cytoskeletal assembly and as a trans-dominant inhibitor of integrin receptor function in mouse keratinocytes. J Cell Biol. 1998;142(5):1357-1369. (Pubitemid 28429116)
16. Conti FJ, Rudling RJ, Robson A, Hodivala-Dilke KM. alpha3beta1-integrin regulates hair follicle but not interfollicular morphogenesis in adult epidermis. J Cell Sci. 2003;116(pt 13):2737-2747. (Pubitemid 36868925)
17. Margadant C, Raymond K, Kreft M, Sachs N, Janssen H, Sonnenberg A. Integrin alpha3beta1 inhibits directional migration and wound re-epithelialization in the skin. J Cell Sci. 2009;122(pt 2):278-288.
18. Yauch RL, Berditchevski F, Harler MB, Reichner J, Hemler ME. Highly stoichiometric, stable, and specific association of integrin α3β1 with CD151 provides a major link to phosphatidylinositol 4-kinase, and may regulate cell migration. Mol Biol Cell. 1998;9(10):2751-2765. (Pubitemid 28473659)
19. Sachs N, et al. Kidney failure in mice lacking the tetraspanin CD151. J Cell Biol. 2006;175(1):33-39. (Pubitemid 44537196)
20. El-Aouni C, et al. Podocyte-specific deletion of integrin-linked kinase results in severe glomerular basement membrane alterations and progressive glomerulosclerosis. J Am Soc Nephrol. 2006;17(5):1334-1344. (Pubitemid 43673413)
21. Miner JH, Li C. Defective glomerulogenesis in the absence of laminin alpha5 demonstrates a developmental role for the kidney glomerular basement membrane. Dev Biol. 2000;217(2):278-289. (Pubitemid 30060876)
22. Kanasaki K, et al. Integrin beta1-mediated matrix assembly and signaling are critical for the normal development and function of the kidney glomerulus. Dev Biol. 2008;313(2):584-593.
23. Pozzi A, et al. Beta1-integrin expression by podocytes is required to maintain glomerular structural integrity. Dev Biol. 2008;316(2):288-301.
24. Sachs N, et al. Blood pressure influences end-stage renal disease of Cd151 knockout mice. J Clin Invest. 2012;122(1):348-358.
25. Baleato RM, Guthrie PL, Gubler MC, Ashman LK, Roselli S. Deletion of CD151 results in a strain-dependent glomerular disease due to severe alterations of the glomerular basement membrane. Am J Pathol. 2008;173(4):927-937.
26. Kaplan JM, et al. Mutations in ACTN4, encoding alpha-actinin-4, cause familial focal segmental glomerulosclerosis. Nat Genet. 2000;24(3):251-256. (Pubitemid 30132192)
27. Zenker M, et al. Human laminin beta2 deficiency causes congenital nephrosis with mesangial sclerosis and distinct eye abnormalities. Hum Mol Genet. 2004;13(21):2625-2632. (Pubitemid 39485411)
28. Karamatic Crew V, et al. CD151, the first member of the tetraspanin (TM4) superfamily detected on erythrocytes, is essential for the correct assembly of human basement membranes in kidney and skin. Blood. 2004;104(8):2217-2223.
29. Takemoto M, et al. A new method for large scale isolation of kidney glomeruli from mice. Am J Pathol. 2002;161(3):799-805. (Pubitemid 34988366)
30. Kazarov AR, Yang X, Stipp CS, Sehgal B, Hemler ME. An extracellular site on tetraspanin CD151 determines alpha3 and alpha6 integrin-dependent cellular morphology. J Cell Biol. 2002;158(7):1299-1309.
31. Serru V, et al. Selective tetraspan-integrin complexes (CD81/alpha4beta1, CD151/alpha3beta1, CD151/alpha6beta1) under conditions disrupting tetraspan interactions. Biochem J. 1999;340(pt 1):103-111. (Pubitemid 29251096)
32. Yauch RL, Kazarov AR, Desai B, Lee RT, Hemler ME. Direct extracellular contact between integrin alpha(3)beta(1) and TM4SF protein CD151. J Biol Chem. 2000;275(13):9230-9238. (Pubitemid 30185141)
33. Nagae M, et al. Crystal structure of α5β1 integrin ectodomain: Atomic details of the fibronectin receptor. J Cell Biol. 2012;197(1):131-140.
34. Berditchevski F, Gilbert E, Griffiths MR, Fitter S, Ashman L, Jenner SJ. Analysis of the CD151-alpha3beta1 integrin and CD151-tetraspanin interactions by mutagenesis. J Biol Chem. 2001;276(44):41165-41174.
35. Caramelo JJ, Parodi AJ. Getting in and out from calnexin/calreticulin cycles. J Biol Chem. 2008;283(16):10221-10225.
36. Lenter M, Vestweber D. The integrin chains beta1 and alpha6 associate with the chaperone calnexin prior to integrin assembly. J Biol Chem. 1994;269(16):12263-12268.
37. Egan ME, et al. Curcumin, a major constituent of turmeric, corrects cystic fibrosis defects. Science. 2004;304(5670):600-602. (Pubitemid 38541921)
38. Wang X, Koulov AV, Kellner WA, Riordan JR, Balch WE. Chemical and biological folding contribute to temperature-sensitive DeltaF508 CFTR trafficking. Traffic. 2008;9(11):1878-1893.
39. Bernier V, Bichet DG, Bouvier M. Pharmacological chaperone action on G-protein-coupled receptors. Curr Opin Pharmacol. 2004;4(5):528-533. (Pubitemid 40533016)
40. Smith MH, Ploegh HL, Weissman JS. Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science. 2011;334(6059):1086-1090.
41. Lederkremer GZ. Glycoprotein folding, quality control and ER-associated degradation. Curr Opin Struct Biol. 2009;19(5):515-523.
42. Has C, et al. Integrin α 3 mutations with kidney, lung, and skin disease. N Engl J Med. 2012;366(16):1508-1514.
43. Margadant C, Frijns E, Wilhelmsen K, Sonnenberg A. Regulation of hemidesmosome (dis-)assembly by growth factor receptors. Curr Opin Cell Biol. 2008;20(5):589-596.
44. Margadant C, Charafeddine RA, Sonnenberg A. Unique and redundant functions of integrins in the epidermis. FASEB J. 2010;24(11):4133-4152.
45. Byron A, Humphries JD, Askari JA, Craig SE, Mould AP, Humphries MJ. Anti-integrin monoclonal antibodies. J Cell Sci. 2009;122(pt 22):4009-4011.
46. Nelson EJ, Li J, Mitchell WB, Chandy M, Srivastava A, Coller BS. Three novel beta-propeller mutations causing Glanzmann thrombasthenia result in production of normally stable pro-alphaIIb, but variably impaired progression of pro-alphaIIbbeta3 from endoplasmic reticulum to Golgi. J Thromb Haemost. 2005;3(12):2773-2783. (Pubitemid 41819807)
47. Mitchell WB, Li J, French DL, Coller BS. alphaIIb-beta3 biogenesis is controlled by engagement of alphaIIb in the calnexin cycle via the N15-linked glycan. Blood. 2006;107(7):2713-2719.
48. Vogt G, Vogt B, Chuzhanova N, Julenius K, Cooper DN, Casanova JL. Gain-of-glycosylation mutations. Curr Opin Genet Dev. 2007;17(3):245-251. (Pubitemid 46843552)
49. Vogt G, et al. Gains of glycosylation comprise an unexpectedly large group of pathogenic mutations. Nat Genet. 2005;37(7):692-700. (Pubitemid 41754885)
50. Back AL, Kerkering M, Baker D, Bauer TR, Embree LJ, Hickstein DD. A point mutation associated with leukocyte adhesion deficiency type 1 of moderate severity. Biochem Biophys Res Commun. 1993;193(3):912-918. (Pubitemid 23209681)
51. Delwel GO, et al. Distinct and overlapping ligand specificities of the alpha3Abeta1 and alpha6Abeta1 integrins: recognition of laminin isoforms. Mol Biol Cell. 1994;5(2):203-215. (Pubitemid 24108466)
52. De Melker AA, et al. The A and B variants of the alpha3 integrin subunit: tissue distribution and functional characterization. Lab Invest. 1997;76(4):547-563. (Pubitemid 27176108)
53. Ports MO, Nagle RB, Pond GD, Cress AE. Extracellular engagement of alpha6 integrin inhibited urokinase-type plasminogen activator-mediated cleavage and delayed human prostate bone metastasis. Cancer Res. 2009;69(12):5007-5014.
54. Nannya Y, et al. A robust algorithm for copy number detection using high-density oligonueclotide single nucleotide polymorphism genotyping arrays. Cancer Res. 2005;65(14):6071-6079. (Pubitemid 40994391)