Nemo-like kinase inhibits osteoblastogenesis by suppressing bone morphogenetic protein and Wnt canonical signaling

Journal of Cellular Biochemistry

Volumn 113, Issue 2, 2012, Pages 449-456

  Zanotti, Stefano ^a,b   Canalis, Ernesto ^a,b  

^a SAINT FRANCIS HOSPITAL AND MEDICAL CENTER   (United States)

^b UNIVERSITY OF CONNECTICUT SCHOOL OF MEDICINE   (United States)

Author keywords

BMP; Nlk; Osteoblasts; Smad; ST 2; Wnt

Indexed keywords

ALKALINE PHOSPHATASE; BETA CATENIN; BONE MORPHOGENETIC PROTEIN 2; NEMO LIKE KINASE; OSTEOCALCIN; PHOSPHOTRANSFERASE; SMAD1 PROTEIN; SMALL INTERFERING RNA; T CELL FACTOR PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; WNT3 PROTEIN; WNT3A PROTEIN;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; LYMPHOCYTE TRANSFORMATION; MOUSE; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STROMA CELL;

ANIMALS; BONE MORPHOGENETIC PROTEIN 2; CELL DIFFERENTIATION; CELLS, CULTURED; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; OSTEOBLASTS; SMAD PROTEINS; TRANSFORMING GROWTH FACTOR BETA; WNT SIGNALING PATHWAY; WNT3A PROTEIN;

MAMMALIA;

EID: 84855545745     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.23365     Document Type: Article

References (40)

1. Bianco P, Gehron RP. 2000. Marrow stromal stem cells. J Clin Invest 105:1663-1668. (Pubitemid 30421745)
2. Canalis E, Deregowski V, Pereira RC, Gazzerro E. 2005. Signals that determine the fate of osteoblastic cells. J Endocrinol Invest 28:3-7.
3. Chen AE, Ginty DD, Fan CM. 2005. Protein kinase A signalling via CREB controls myogenesis induced by Wnt proteins. Nature 433:317-322.
4. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498. (Pubitemid 32494397)
5. Gazzerro E, Pereira RC, Jorgetti V, Olson S, Economides AN, Canalis E. 2005. Skeletal overexpression of gremlin impairs bone formation and causes osteopenia. Endocrinology 146:655-665. (Pubitemid 40129821)
6. Ishitani T, Ninomiya-Tsuji J, Nagai S, Nishita M, Meneghini M, Barker N, Waterman M, Boweman B, Clevers H, Shibuya H, Matsumoto K. 1999. The TAK1-NLK-MAPK-related pathway antagonizes signalling between beta-catenin and transcription factor TCF. Nature 399:798-802. (Pubitemid 29293177)
7. Ishitani T, Ninomiya-Tsuji J, Matsumoto K. 2003. Regulation of lymphoid enhancer factor 1/T-cell factor by mitogen-activated protein kinase-related Nemo-like kinase-dependent phosphorylation in Wnt/beta-catenin signaling. Mol Cell Biol 23:1379-1389. (Pubitemid 36177046)
8. Ishitani S, Inaba K, Matsumoto K, Ishitani T. 2011. Homodimerization of Nemo-like kinase is essential for activation and nuclear localization. Mol Biol Cell 22:266-277.
9. Itasaki N, Hoppler S. 2010. Crosstalk between Wnt and bone morphogenic protein signaling: A turbulent relationship. Dev Dyn 239:16-33.
10. Javelaud D, Mauviel A. 2005. Crosstalk mechanisms between the mitogen-activated protein kinase pathways and Smad signaling downstream of TGF-beta: Implications for carcinogenesis. Oncogene 24:5742-5750. (Pubitemid 43086134)
11. Kortenjann M, Nehls M, Smith AJ, Carsetti R, Schuler J, Kohler G, Boehm T. 2001. Abnormal bone marrow stroma in mice deficient for nemo-like kinase, Nlk. Eur J Immunol 31:3580-3587. (Pubitemid 34030970)
12. Kouadjo KE, Nishida Y, Cadrin-Girard JF, Yoshioka M, St-Amand J. 2007. Housekeeping and tissue-specific genes in mouse tissues. BMC Genomics 8:127.
13. Kretzschmar M, Doody J, Massague J. 1997. Opposing BMP and EGF signalling pathways converge on the TGF-beta family mediator Smad1. Nature 389:618-622. (Pubitemid 27446181)
14. Kretzschmar M, Doody J, Timokhina I, Massague J. 1999. A mechanism of repression of TGFbeta/ Smad signaling by oncogenic Ras. Genes Dev 13:804-816. (Pubitemid 29169840)
15. Li M, Wang H, Huang T, Wang J, Ding Y, Li Z, Zhang J, Li L. 2010. TAB2 scaffolds TAK1 and NLK in repressing canonical Wnt signaling. J Biol Chem 285:13397-13404.
16. Lian J, Stewart C, Puchacz E, Mackowiak S, Shalhoub V, Collart D, Zambetti G, Stein G. 1989. Structure of the rat osteocalcin gene and regulation of vitamin D-dependent expression. Proc Natl Acad Sci USA 86:1143-1147. (Pubitemid 19061510)
17. MacDonald BT, Tamai K, He X. 2009. Wnt/beta-catenin signaling: Components, mechanisms, and diseases. Dev Cell 17:9-26.
18. Massague J, Chen YG. 2000. Controlling TGF-beta signaling. Genes Dev 14:627-644.
19. McCarthy TL, Centrella M, Canalis E. 1990. Cortisol inhibits the synthesis of insulin-like growth factor-I in skeletal cells. Endocrinology 126:1569-1575. (Pubitemid 20095765)
20. Merino C, Penney J, Gonzalez M, Tsurudome K, Moujahidine M, O'Connor MB, Verheyen EM, Haghighi P. 2009. Nemo kinase interacts with Mad to coordinate synaptic growth at the Drosophila neuromuscular junction. J Cell Biol 185:713-725.
21. Miyata Y, Nishida E. 1999. Distantly related cousins of MAP kinase: Biochemical properties and possible physiological functions. Biochem Biophys Res Commun 266:291-295. (Pubitemid 30028660)
22. Nakashima A, Katagiri T, Tamura M. 2005. Cross-talk between Wnt and bone morphogenetic protein 2 (BMP-2) signaling in differentiation pathway of C2C12 myoblasts. J Biol Chem 280:37660-37668. (Pubitemid 41642374)
23. Nazarenko I, Pires R, Lowe B, Obaidy M, Rashtchian A. 2002. Effect of primary and secondary structure of oligodeoxyribonucleotides on the fluorescent properties of conjugated dyes. Nucleic Acids Res 30:2089-2195.
24. Nazarenko I, Lowe B, Darfler M, Ikonomi P, Schuster D, Rashtchian A. 2002. Multiplex quantitative PCR using self-quenched primers labeled with a single fluorophore. Nucleic Acids Res 30:e37.
25. Nifuji A, Ideno H, Ohyama Y, Takanabe R, Araki R, Abe M, Noda M, Shibuya H. 2010. Nemo-like kinase (NLK) expression in osteoblastic cells and suppression of osteoblastic differentiation. Exp Cell Res 316:1127-1136.
26. Nohe A, Hassel S, Ehrlich M, Neubauer F, Sebald W, Henis YI, Knaus P. 2002. The mode of bone morphogenetic protein (BMP) receptor oligomerization determines different BMP-2 signaling pathways. J Biol Chem 277:5330-5338. (Pubitemid 34968578)
27. Sapkota G, Alarcon C, Spagnoli FM, Brivanlou AH, Massague J. 2007. Balancing BMP signaling through integrated inputs into the Smad1 linker. Mol Cell 25:441-454. (Pubitemid 46199289)
28. Sharp PA. 2001. RNA interference-2001. Genes Dev 15:485-490.
29. Smit L, Baas A, Kuipers J, Korswagen H, van de WM, Clevers H. 2004. Wnt activates the Tak1/Nemo-like kinase pathway. J Biol Chem 279:17232-17240. (Pubitemid 38560481)
30. Takada I, Mihara M, Suzawa M, Ohtake F, Kobayashi S, Igarashi M, Youn MY, Takeyama K, Nakamura T, Mezaki Y, Takezawa S, Yogiashi Y, Kitagawa H, Yamada G, Takada S, Minami Y, Shibuya H, Matsumoto K, Kato S. 2007. A histone lysine methyltransferase activated by non-canonical Wnt signalling suppresses PPAR-gamma transactivation. Nat Cell Biol 9:1273-1285. (Pubitemid 350042359)
31. Westendorf JJ, Kahler RA, Schroeder TM. 2004. Wnt signaling in osteoblasts and bone diseases. Gene 341:19-39. (Pubitemid 39335880)
32. Yamada M, Ohnishi J, Ohkawara B, Iemura S, Satoh K, Hyodo-Miura J, Kawachi K, Natsume T, Shibuya H. 2006. NARF, an nemo-like kinase (NLK)- associated ring finger protein regulates the ubiquitylation and degradation of T cell factor/lymphoid enhancer factor (TCF/LEF). J Biol Chem 281:20749-20760. (Pubitemid 44115416)
33. Young CS, Kitamura M, Hardy S, Kitajewski J. 1998. Wnt-1 induces growth, cytosolic beta-catenin, and Tcf/Lef transcriptional activation in Rat-1 fibroblasts. Mol Cell Biol 18:2474-2485. (Pubitemid 28183417)
34. Yu HC, Wu TC, Chen MR, Liu SW, Chen JH, Lin KM. 2010. Mechanical stretching induces osteoprotegerin in differentiating C2C12 precursor cells through noncanonical Wnt pathways. J Bone Miner Res 25:1128-1137.
35. Zanotti S, Smerdel-Ramoya A, Stadmeyer L, Canalis E. 2008. Activation of the ERK pathway in osteoblastic cells, role of gremlin and BMP-2. J Cell Biochem 104:1421-1426. (Pubitemid 351961711)
36. Zanotti S, Smerdel-Ramoya A, Stadmeyer L, Durant D, Radtke F, Canalis E. 2008. Notch inhibits osteoblast differentiation and causes osteopenia. Endocrinology 149:3890-3899.
37. Zawel L, Dai JL, Buckhaults P, Zhou S, Kinzler KW, Vogelstein B, Kern SE. 1998. Human Smad3 and Smad4 are sequence-specific transcription activators. Mol Cell 1:611-617. (Pubitemid 128374697)
38. Zeng YA, Verheyen EM. 2004. Nemo is an inducible antagonist of Wingless signaling during Drosophila wing development. Development 131:2911-2920. (Pubitemid 38997279)
39. Zeng YA, Rahnama M, Wang S, Sosu-Sedzorme W, Verheyen EM. 2007. Drosophila Nemo antagonizes BMP signaling by phosphorylation of Mad and inhibition of its nuclear accumulation. Development 134:2061-2071. (Pubitemid 46979793)
40. Zhao M, Qiao M, Harris SE, Oyajobi BO, Mundy GR, Chen D. 2004. Smurf1 inhibits osteoblast differentiation and bone formation in vitro and in vivo. J Biol Chem 279:12854-12859. (Pubitemid 38445859)