The hippo signaling pathway is required for salivary gland development and its dysregulation is associated with sjogren's syndrome

Laboratory Investigation

Volumn 93, Issue 11, 2013, Pages 1203-1218

  Enger, Tone B ^a   Samad Zadeh, Arman ^b   Bouchie, Meghan P ^b   Skarstein, Kathrine ^c   Galtung, Hilde K ^a   Mera, Toshiyuki ^d   Walker, Janice ^e   Menko, A Sue ^e   Varelas, Xaralabos ^b   Faustman, Denise L ^d   Jensen, Janicke L ^a   A Kukuruzinska, Maria ^b  

^a UNIVERSITY OF OSLO   (Norway)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

E cadherin adhesion; Hippo signaling; salivary gland; Sjogren's syndrome; TAZ

Indexed keywords

SMALL INTERFERING RNA; UVOMORULIN; ALPHA CATENIN; CADHERIN; HIPPO PROTEIN, MOUSE; LATS2 PROTEIN, MOUSE; PROTEIN SERINE THREONINE KINASE; TAZ PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN;

ACINAR CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOIMMUNE DISEASE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HIPPO SIGNALING; HUMAN; HUMAN TISSUE; MICROSCOPE; MORPHOGENESIS; MOUSE; NONHUMAN; ORGAN CULTURE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SALIVARY GLAND; SALIVARY GLAND DUCT; SIGNAL TRANSDUCTION; SJOEGREN SYNDROME; SUBMANDIBULAR GLAND; TRANSCRIPTION REGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CASE CONTROL STUDY; CELL POLARITY; DISEASE MODEL; GENETICS; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHOSPHORYLATION; SJOGREN'S SYNDROME;

ALPHA CATENIN; ANIMALS; CADHERINS; CASE-CONTROL STUDIES; CELL POLARITY; DISEASE MODELS, ANIMAL; HUMANS; MICE; MICE, INBRED NOD; MORPHOGENESIS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SJOGREN'S SYNDROME; SUBMANDIBULAR GLAND; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84886771988     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2013.114     Document Type: Article

References (49)

1. Jonsson R, Bolstad AI, Brokstad KA, et al. Sjogren's syndrome-a plethora of clinical and immunological phenotypes with a complex genetic background. Ann N Y Acad Sci 2007;1108:433-447. (Pubitemid 47528757)
2. Hatzopoulos S, Amoroso C, Aimoni C, et al. Hearing loss evaluation of Sjogren's syndrome using distortion product otoacoustic emissions. Acta Otolaryngol Suppl 2002;548:20-25. (Pubitemid 34913449)
3. Boki KA, Ioannidis JP, Segas JV, et al. How significant is sensorineural hearing loss in primary Sjogren's syndrome? An individually matched case-control study. J Rheumatol 2001;28:798-801. (Pubitemid 32246949)
4. Ferrer JP, Biurrun O, Lorente J, et al. Auditory function in young patients with type 1 diabetes mellitus. Diabetes Res Clin Pract 1991; 11:17-22.
5. Fukushima H, Cureoglu S, Schachern PA, et al. Cochlear changes in patients with type 1 diabetes mellitus. Otolaryngol Head Neck Surg 2005;133:100-106. (Pubitemid 40980970)
6. Beppu T, Sasaki T, Kawabata K, et al. Usefulness and limitations in ultrasonography for diagnosing neck lymph node metastases in patients with hypopharyngeal squamous cell carcinoma: comparison with pathological findings following neck dissection. Nihon Jibiinkoka Gakkai Kaiho 2005;108:794-800. (Pubitemid 41265242)
7. Lonyai A, Kodama S, Burger D, et al. The promise of Hox11\+ stem cells of the spleen for treating autoimmune diseases. Horm Metab Res 2008;40:137-146. (Pubitemid 351363425)
8. Lonyai A, Kodama S, Burger D, et al. Fetal Hox11 expression patterns predict defective target organs: a novel link between developmental biology and autoimmunity. Immunol Cell Biol 2008;86:301-309. (Pubitemid 351668000)
9. Jaskoll T, Zhou YM, Chai Y, et al. Embryonic submandibular gland morphogenesis: stage-specific protein localization of FGFs, BMPs, Pax6 and Pax9 in normal mice and abnormal SMG phenotypes in FgfR2-IIIc(\+/Delta), BMP7(f/r) and Pax6(f/r) mice. Cells Tissues Organs 2002;170:83-98. (Pubitemid 33151582)
10. Haara O, Koivisto T, Miettinen PJ. EGF-receptor regulates salivary gland branching morphogenesis by supporting proliferation and maturation of epithelial cells and survival of mesenchymal cells. Differentiation 2009;77:298-306.
11. Entesarian M, Matsson H, Klar J, et al. Mutations in the gene encoding fibroblast growth factor 10 are associated with aplasia of lacrimal and salivary glands. Nat Genet 2005;37:125-127.
12. Rebustini IT, Patel VN, Stewart JS, et al. Laminin alpha5 is necessary for submandibular gland epithelial morphogenesis and influences FGFR expression through beta1 integrin signaling. Dev Biol 2007;308:15-29. (Pubitemid 47087775)
13. Daley WP, Gervais EM, Centanni SW, et al. ROCK1-directed basement membrane positioning coordinates epithelial tissue polarity. Development 2012;139:411-422.
14. Knox SM, Lombaert IM, Reed X, et al. Parasympathetic innervation maintains epithelial progenitor cells during salivary organogenesis. Science 2010;329:1645-1647.
15. Patel VN, Rebustini IT, Hoffman MP. Salivary gland branching morphogenesis. Differentiation 2006;74:349-364. (Pubitemid 44215407)
16. Walker JL, Menko AS, Khalil S, et al. Diverse roles of E-cadherin in the morphogenesis of the submandibular gland: insights into the formation of acinar and ductal structures. Dev Dyn 2008;237: 3128-3141.
17. Cherrett C, Furutani-Seiki M, Bagby S. The Hippo pathway: key interaction and catalytic domains in organ growth control, stem cell self-renewal and tissue regeneration. Essays Biochem 2012;53: 111-127.
18. Varelas X, Wrana JL. Coordinating developmental signaling: novel roles for the Hippo pathway. Trends Cell Biol 2012;22:88-96.
19. Zhao B, Lei QY, Guan KL. The Hippo-YAP pathway: new connections between regulation of organ size and cancer. Curr Opin Cell Biol 2008;20:638-646.
20. Halder G, Johnson RL. Hippo signaling: growth control and beyond. Development 2011;138:9-22.
21. Lei QY, Zhang H, Zhao B, et al. TAZ promotes cell proliferation and epithelial-mesenchymal transition and is inhibited by the hippo pathway. Mol Cell Biol 2008;28:2426-2436. (Pubitemid 351429986)
22. Silvis MR, Kreger BT, Lien WH, et al. Alpha-catenin is a tumor suppressor that controls cell accumulation by regulating the localization and activity of the transcriptional coactivator Yap1. Sci Signal 2011;4, ra33.
23. Kim NG, Koh E, Chen X, et al. E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components. Proc Natl Acad Sci USA. 2011;108:11930-11935.
24. Schlegelmilch K, Mohseni M, Kirak O, et al. Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 2011;144: 782-795.
25. Varelas X, Samavarchi-Tehrani P, Narimatsu M, et al. The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-beta-SMAD pathway. Dev Cell 2010;19: 831-844.
26. Menko AS, Zhang L, Schiano F, et al. Regulation of cadherin junctions during mouse submandibular gland development. Dev Dyn 2002;224: 321-333. (Pubitemid 34700951)
27. Cutler LS, Mooradian BA. Lumen formation during development of the rat submandibular gland. J Dent Res 1987;66:1559-1562.
28. Heida Y, Nakanishi Y. Epithelial morphogenesis in mouse embryonic submandibular gland: its relationships to the tissue organization of epithelium and mesenchyme. Dev Growth Differ 1997; 39:1-8. (Pubitemid 27120216)
29. Remue E, Meerschaert K, Oka T, et al. TAZ interacts with zonula occludens-1 and-2 proteins in a PDZ-1 dependent manner. FEBS Lett 2010;584:4175-4180.
30. Oka T, Remue E, Meerschaert K, et al. Functional complexes between YAP2 and ZO-2 are PDZ domain-dependent, and regulate YAP2 nuclear localization and signalling. Biochem J 2010;432: 461-472.
31. Soyfoo MS, Steinfeld S, Delporte C. Usefulness of mouse models to study the pathogenesis of Sjogren's syndrome. Oral Dis 2007;13: 366-375. (Pubitemid 46934581)
32. Kuroda S, Fukata M, Nakagawa M, et al. Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin-mediated cell-cell adhesion. Science 1998;281:832-835. (Pubitemid 28376045)
33. Abdel-Wahab N, Weston BS, Roberts T, et al. Connective tissue growth factor and regulation of the mesangial cell cycle: role in cellular hypertrophy. J Am Soc Nephrol 2002;13:2437-2445.
34. Kodama S, Kuhtreiber W, Fujimura S, et al. Islet regeneration during the reversal of autoimmune diabetes in NOD mice. Science 2003;302:1223-1227. (Pubitemid 37421029)
35. Cha S, van Blockland SC, Versnel MA, et al. Abnormal organogenesis in salivary gland development may initiate adult onset of autoimmune exocrinopathy. Exp Clin Immunogenet 2001;18:143-160. (Pubitemid 32830559)
36. Price EJ, Venables PJ. The etiopathogenesis of Sjogren's syndrome. Arthritis Rheum 1995;25:117-133.
37. Ewert P, Aguilera S, Alliende C, et al. Disruption of tight junction structure in salivary glands from Sjogren's syndrome patients is linked to proinflammatory cytokine exposure. Arthritis Rheum 2010; 62:1280-1289.
38. Velozo J, Aguilera S, Alliende C, et al. Severe alterations in expression and localisation of {alpha}6{beta}4 integrin in salivary gland acini from patients with Sjogren syndrome. Ann Rheum Dis 2009;68:991-996.
39. Barrera MJ, Sanchez M, Aguilera S, et al. Aberrant localization of fusion receptors involved in regulated exocytosis in salivary glands of Sjogren's syndrome patients is linked to ectopic mucin secretion. J Autoimmun 2012;39:83-92.
40. Delaleu N, Jonsson MV, Appel S, et al. New concepts in the pathogenesis of Sjogren's syndrome. Rheum Dis Clin North Am 2008;34:833-845, vii.
41. Hoffman MP, Kidder BL, Steinberg ZL, et al. Gene expression profiles of mouse submandibular gland development: FGFR1 regulates branching morphogenesis in vitro through BMP-and FGF-dependent mechanisms. Development 2002;129:5767-5778. (Pubitemid 36054619)
42. Mitani A, Nagase T, Fukuchi K, et al. Transcriptional coactivator with PDZ-binding motif is essential for normal alveolarization in mice. Am J Respir Crit Care Med 2009;180:326-338.
43. Steinfeld S, Cogan E, King LS, et al. Abnormal distribution of aquaporin-5 water channel protein in salivary glands from Sjogren's syndrome patients. Lab Invest 2001;81:143-148. (Pubitemid 32176377)
44. Perez P, Aguilera S, Olea N, et al. Aberrant localization of ezrin correlates with salivary acini disorganization in Sjogren's Syndrome. Rheumatology 2010;49:915-923.
45. Bahamondes V, Albornoz A, Aguilera S, et al. Changes in Rab3D expression and distribution in the acini of Sjogren's syndrome patients are associated with loss of cell polarity and secretory dysfunction. Arthritis Rheum 2011;63:3126-3135.
46. Tinkle CL, Lechler T, Pasolli HA, et al. Conditional targeting of E-cadherin in skin: Insights into hyperproliferative and degenerative responses. Proc Natl Acad Sci 2003;101:552-557. (Pubitemid 38084674)
47. Vasioukhin VBC, Degenstein L, Wise B, et al. Hyperproliferation and defects in epithelial polarity upon conditional ablation of alphacatenin in skin. Cell 2001;104:605-617. (Pubitemid 32201954)
48. Balkwill F, Mantovani A. Inflammation and cancer: back to Virchow? Lancet 2001;357:539-545. (Pubitemid 32173595)
49. Price EJ, Venables PJ. The etiopathogenesis of Sjogren's syndrome. Semin Arthritis Rheum 1995;25:117-133.