Cellular and Molecular Life Sciences

, Volume 69, Issue 3, pp 423–434 | Cite as

Four-and-a-half LIM domains protein 2 (FHL2) is associated with the development of craniofacial musculature in the teleost fish Sparus aurata

  • Marta S. Rafael
  • Vincent Laizé
  • Anabela Bensimon-Brito
  • Ricardo B. Leite
  • Roland Schüle
  • M. Leonor Cancela
Research Article

Abstract

Four-and-a-half LIM domains protein 2 (FHL2) is involved in major cellular mechanisms such as regulation of gene transcription and cytoskeleton modulation, participating in physiological control of cardiogenesis and osteogenesis. Knowledge on underlying mechanisms is, however, limited. We present here new data on FHL2 protein and its role during vertebrate development using a marine teleost fish, the gilthead seabream (Sparus aurata L.). In silico comparison of vertebrate protein sequences and prediction of LIM domain three-dimensional structure revealed a high degree of conservation, suggesting a conserved function throughout evolution. Determination of sites and levels of FHL2 gene expression in seabream indicated a central role for FHL2 in the development of heart and craniofacial musculature, and a potential role in tissue calcification. Our data confirmed the key role of FHL2 protein during vertebrate development and gave new insights into its particular involvement in craniofacial muscle development and specificity for slow fibers.

Keywords

Four-and-a-half LIM domains protein 2, FHL2 Teleost fish Gene expression patterns Muscle development 3D protein structure 

Abbreviations

CDS

Coding sequence

DPF

Days post fertilization

EST

Expressed sequence tag

FHL2

Four-and-a-half LIM domains protein 2

HPF

Hours post fertilization

LIM

Lin11, Isl-1 and Mec-3 proteins

WGS

Whole genome shotgun

Supplementary material

18_2011_754_MOESM1_ESM.jpg (201 kb)
Supplementary Fig. S1 (JPG 200 kb)
18_2011_754_MOESM2_ESM.doc (54 kb)
Supplementary Fig. S2 (DOC 54 kb)
18_2011_754_MOESM3_ESM.doc (58 kb)
Supplementary Fig. S3. (DOC 57 kb)
18_2011_754_MOESM4_ESM.doc (108 kb)
Fig. S4 Taxonomic tree of the 38 species included in FHL2 protein analysis, according to Taxonomy Browser at NCBI; * indicates species with evidence of a second gene. (DOC 107 kb)
18_2011_754_MOESM5_ESM.doc (40 kb)
Supplementary Fig. S5 (DOC 39 kb)
18_2011_754_MOESM6_ESM.jpg (661 kb)
Supplementary Fig. S6 (JPG 661 kb)

References

  1. 1.
    Kadrmas JL, Beckerle MC (2004) The LIM domain: from the cytoskeleton to the nucleus. Nat Rev Mol Cell Biol 5:920–931PubMedCrossRefGoogle Scholar
  2. 2.
    Lumsden A (1995) Neural development. A ‘LIM code’ for motor neurons? Curr Biol 5:491–495PubMedCrossRefGoogle Scholar
  3. 3.
    Weiskirchen R, Pino JD, Macalma T, Bister K, Beckerle MC (1995) The cysteine-rich protein family of highly related LIM domain proteins. J Biol Chem 270:28946–28954PubMedCrossRefGoogle Scholar
  4. 4.
    Chu P-H, Bardwell WM, Gu Y, Ross J Jr, Chen J (2000) FHL2 (SLIM3) is not essential for cardiac development and function. Mol Cell Biol 20:7460–7462PubMedCrossRefGoogle Scholar
  5. 5.
    Müller JM, Isele U, Metzger E, Rempel A, Moser M, Pscherer A, Breyer T, Holubarsch C, Buettner R, Schüle R (2000) FHL2, a novel tissue-specific coactivator of the androgen receptor. EMBO J 19:359–369PubMedCrossRefGoogle Scholar
  6. 6.
    Canault M, Tellier E, Bonardo B, Mas E, Aumailley M, Juhan-Vague I, Nalbone G, Peiretti F (2006) FHL2 interacts with both ADAM-17 and the cytoskeleton and regulates ADAM-17 localization and activity. J Cell Physiol 208:363–372PubMedCrossRefGoogle Scholar
  7. 7.
    Müller JM, Metzger E, Greschik H, Bosserhoff A-K, Mercep L, Buettner R, Schüle R (2002) The transcriptional coactivator FHL2 transmits Rho signals from the cell membrane into the nucleus. EMBO J 21:736–748PubMedCrossRefGoogle Scholar
  8. 8.
    Johannessen M, Moller S, Hansen T, Moens U, Ghelue MV (2006) The multifunctional roles of the four-and-a-half-LIM only protein FHL2. Cell Mol Life Sci 63:268–284PubMedCrossRefGoogle Scholar
  9. 9.
    Bach I (2000) The LIM domain: regulation by association. Mech Dev 91:5–17PubMedCrossRefGoogle Scholar
  10. 10.
    Martin B, Schneider R, Janetzky S, Waibler Z, Pandur P, Kuhl M, Behrens J, von der Mark K, Starzinski-Powitz A, Wixler V (2002) The LIM-only protein FHL2 interacts with β-catenin and promotes differentiation of mouse myoblasts. J Cell Biol 159:113–122PubMedCrossRefGoogle Scholar
  11. 11.
    Günther T, Poli C, Müller JM, Catala-Lehnen P, Schinke T, Yin N, Vomstein S, Amling M, Schüle R (2005) Fhl2 deficiency results in osteopenia due to decreased activity of osteoblasts. EMBO J 24:3049–3056PubMedCrossRefGoogle Scholar
  12. 12.
    Labalette C, Nouet Y, Sobczak-Thepot J, Armengol C, Levillayer F, Gendron M-C, Renard C-A, Regnault B, Chen J, Buendia M-A, Wei Y (2008) The LIM-only protein FHL2 regulates cyclin D1 expression and cell proliferation. J Biol Chem 238:15201–15208CrossRefGoogle Scholar
  13. 13.
    Morlon A, Sassone-Corsi P (2003) The LIM-only protein FHL2 is a serum-inducible transcriptional coactivator of AP-1. Proc Natl Acad Sci USA 100:3977–3982PubMedCrossRefGoogle Scholar
  14. 14.
    Genini M, Schwalbe P, Scholl FA, Remppis A, Mattei MG, Schafer BW (1997) Subtractive cloning and characterization of DRAL, a novel LIM-domain protein down-regulated in rhabdomyosarcoma. DNA Cell Biol 16:433–442PubMedCrossRefGoogle Scholar
  15. 15.
    Gabriel B, Fischer DC, Orlowska-Volk M, Hausen A, Schüle R, Müller JM, Hasenburg A (2006) Expression of the transcriptional coregulator FHL2 in human breast cancer: a clinicopathologic study. J Soc Gynecol Investig 13:69–75PubMedCrossRefGoogle Scholar
  16. 16.
    Gullotti L, Hirner S, Merckelback-Bruse S, Fishel R, Schüle R, Buettner R (2004) LIM only protein FHL2 expression in colorectal cancer. AACR Meeting Abstracts 45:213Google Scholar
  17. 17.
    Heemers HV, Regan KM, Dehm SM, Tindall DJ (2007) Androgen induction of the androgen receptor coactivator four-and-a-half LIM domain protein-2: evidence for a role for serum response factor in prostate cancer. Cancer Res 67:10592–10599PubMedCrossRefGoogle Scholar
  18. 18.
    Gabriel B, Mildenberger S, Weisser CW, Metzger E, Gitsch G, Schüle R, Müller JM (2004) Focal adhesion kinase interacts with the transcriptional coactivator FHL2 and both are overexpressed in epithelial ovarian cancer. Anticancer Res 24:921–927PubMedGoogle Scholar
  19. 19.
    Roest Crollius H, Weissenbach J (2005) Fish genomics and biology. Genome Res 15:1675–1682PubMedCrossRefGoogle Scholar
  20. 20.
    Bassett DI, Currie PD (2003) The zebrafish as a model for muscular dystrophy and congenital myopathy. Hum Mol Genet 12:R265–R270PubMedCrossRefGoogle Scholar
  21. 21.
    Johnston IA (1999) Muscle development and growth: potential implications for flesh quality in fish. Aquaculture 177:99–115CrossRefGoogle Scholar
  22. 22.
    Andrades JA, Becerra J, Fernández-Llebrez P (1996) Skeletal deformities in larval juvenile and adult stages of cultured gilthead sea bream (Sparus aurata L.). Aquaculture 141:1–11CrossRefGoogle Scholar
  23. 23.
    Rowlerson A, Radaelli G, Mascarello F, Veggetti A (1997) Regeneration of skeletal muscle in two teleost fish: Sparus aurata and Brachydanio rerio. Cell Tissue Res 289:311–322PubMedCrossRefGoogle Scholar
  24. 24.
    Ramírez-Zarzosa G, Gil F, Latorre R, Ortega A, García-Alcaráz A, Abellán E, Vázquez JM, López-Albors O, Arencibia A, Moreno F (1995) The larval development of lateral musculature in gilthead sea bream Sparus aurata and sea bass Dicentrarchus labrax. Cell Tissue Res 280:217–224CrossRefGoogle Scholar
  25. 25.
    Boukouvala E, Leaver MJ, Favre-Krey L, Theodoridou M, Krey G (2010) Molecular characterization of a gilthead sea bream (Sparus aurata) muscle tissue cDNA for carnitine palmitoyltransferase 1B (CPT1B). Comp Biochem Physiol Part B Biochem Mol Biol 157:189–197CrossRefGoogle Scholar
  26. 26.
    Tiago DM, Laizé V, Cancela ML (2008) Alternatively spliced transcripts of Sparus aurata insulin-like growth factor 1 are differentially expressed in adult tissues and during early development. Gen Comp Endocrinol 157:107–115PubMedCrossRefGoogle Scholar
  27. 27.
    Thisse C, Thisse B, Schilling TF, Postlethwait JH (1993) Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development 119:1203–1215PubMedGoogle Scholar
  28. 28.
    Witten PE, Hansen A, Hall BK (2001) Features of mono- and multinucleated bone resorbing cells of the zebrafish Danio rerio and their contribution to skeletal development, remodeling, and growth. J Morphol 250:197–207PubMedCrossRefGoogle Scholar
  29. 29.
    Simes DC, Williamson MK, Ortiz-Delgado JB, Viegas CSB, Price PA, Cancela ML (2003) Purification of matrix Gla protein from a marine teleost fish, Argyrosomus regius: calcified cartilage and not bone as the primary site of MGP accumulation in fish. J Bone Miner Res 18:244–259PubMedCrossRefGoogle Scholar
  30. 30.
    Notredame C, Higgins DG, Heringa J (2000) T-Coffee: a novel method for fast and accurate multiple sequence alignment. J Mol Biol 302:205–217PubMedCrossRefGoogle Scholar
  31. 31.
    Schneider TD, Stephens RM (1990) Sequence logos—a new way to display consensus sequences. Nucleic Acids Res 18:6097–6100PubMedCrossRefGoogle Scholar
  32. 32.
    Shen M-y, Sali A (2006) Statistical potential for assessment and prediction of protein structures. Protein Sci 15:2507–2524PubMedCrossRefGoogle Scholar
  33. 33.
    Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612PubMedCrossRefGoogle Scholar
  34. 34.
    Silva P, Rowlerson AM, Valente LM, Olmedo M, Monteiro RA, Rocha E (2008) Muscle differentiation in blackspot seabream (Pagellus bogaraveo, Brunnich): histochemical and immunohistochemical study of the fibre types. Tissue Cell 40:447–458PubMedCrossRefGoogle Scholar
  35. 35.
    Hernandez LP, Patterson SE, Devoto SH (2005) The development of muscle fiber type identity in zebrafish cranial muscles. Anat Embryol (Berl) 209:323–334CrossRefGoogle Scholar
  36. 36.
    Chu P-H, Ruiz-Lozano P, Zhou Q, Cai C, Chen J (2000) Expression patterns of FHL/SLIM family members suggest important functional roles in skeletal muscle and cardiovascular system. Mech Dev 95:259–265PubMedCrossRefGoogle Scholar
  37. 37.
    Kong Y, Shelton JM, Rothermel B, Li X, Richardson JA, Bassel-Duby R, Williams RS (2001) Cardiac-specific LIM protein FHL2 modifies the hypertrophic response to β-adrenergic stimulation. Circulation 103:2731–2738PubMedGoogle Scholar
  38. 38.
    Moretti A, Fernandez-Criado MP, Cittolin G, Guidastri R (1999) Manual on hatchery production of seabass and gilthead seabream. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  39. 39.
    Devoto SH, Melancon E, Eisen JS, Westerfield M (1996) Identification of separate slow and fast muscle precursor cells in vivo, prior to somite formation. Development 122:3371–3380PubMedGoogle Scholar
  40. 40.
    Chauvigné F, Cauty C, Rallière C, Rescan PY (2005) Muscle fiber differentiation in fish embryos as shown by in situ hybridization of a large repertoire of muscle-specific transcripts. Dev Dyn 233:659–666PubMedCrossRefGoogle Scholar
  41. 41.
    Fimia GM, De Cesare D, Sassone-Corsi P (2000) A family of LIM-only transcriptional coactivators: tissue-specific expression and selective activation of CREB and CREM. Mol Cell Biol 20:8613–8622PubMedCrossRefGoogle Scholar
  42. 42.
    Chan KK, Tsui SKW, Lee SMY, Luk SCW, Liew CC, Fung KP, Waye MMY, Lee CY (1998) Molecular cloning and characterization of FHL2, a novel LIM domain protein preferentially expressed in human heart. Gene 210:345–350PubMedCrossRefGoogle Scholar
  43. 43.
    Patterson SE, Mook LB, Devoto SH (2008) Growth in the larval zebrafish pectoral fin and trunk musculature. Dev Dyn 237:307–315PubMedCrossRefGoogle Scholar
  44. 44.
    Amann K, Wolf B, Nichols C, Tornig J, Schwarz U, Zeier M, Mall G, Ritz E (1997) Aortic changes in experimental renal failure: hyperplasia or hypertrophy of smooth muscle cells? Hypertension 29:770–775PubMedGoogle Scholar
  45. 45.
    Shi X, Bowlin KM, Garry DJ (2010) Fhl2 interacts with Foxk1 and corepresses Foxo4 activity in myogenic progenitors. Stem Cells 28:462–469PubMedGoogle Scholar
  46. 46.
    Amaar YG, Thompson GR, Linkhart TA, Chen S-T, Baylink DJ, Mohan S (2002) Insulin-like growth factor-binding protein 5 (IGFBP-5) interacts with a four-and-a-half LIM protein 2 (FHL2). J Biol Chem 277:12053–12060PubMedCrossRefGoogle Scholar
  47. 47.
    Wei Y, Renard C-A, Labalette C, Wu Y, Levy L, Neuveut C, Prieur X, Flajolet M, Prigent S, Buendia M-A (2003) Identification of the LIM protein FHL2 as a coactivator of β-catenin. J Biol Chem 278:5188–5194PubMedCrossRefGoogle Scholar
  48. 48.
    Hamidouche Z, Hay E, Vaudin P, Charbord P, Schüle R, Marie PJ, Fromigué O (2008) FHL2 mediates dexamethasone-induced mesenchymal cell differentiation into osteoblasts by activating Wnt/β-catenin signaling-dependent Runx2 expression. FASEB J 22:3813–3822PubMedCrossRefGoogle Scholar
  49. 49.
    Wixler V, Hirner S, Müller JM, Gullotti L, Will C, Kirfel J, Günther T, Schneider H, Bosserhoff A, Schorle H, Park J, Schüle R, Buettner R (2007) Deficiency in the LIM-only protein Fhl2 impairs skin wound healing. J Cell Biol 177:163–172PubMedCrossRefGoogle Scholar
  50. 50.
    Park J, Will C, Martin B, Gullotti L, Friedrichs N, Buettner R, Schneider H, Ludwig S, Wixler V (2008) Deficiency in the LIM-only protein FHL2 impairs assembly of extracellular matrix proteins. FASEB J 22:2508–2520PubMedCrossRefGoogle Scholar
  51. 51.
    Blair JE, Hedges SB (2005) Molecular phylogeny and divergence times of deuterostome animals. Mol Biol Evol 22:2275–2284PubMedCrossRefGoogle Scholar
  52. 52.
    Marques CL, Rafael MS, Cancela ML, Laizé V (2007) Establishment of primary cell cultures from fish calcified tissues. Cytotechnology 55:9–13PubMedCrossRefGoogle Scholar
  53. 53.
    Conceição N, Laizé V, Simões B, Pombinho AR, Cancela ML (2008) Retinoic acid is a negative regulator of matrix Gla protein gene expression in teleost fish Sparus aurata. Biochim Biophys Acta 1779:28–39PubMedGoogle Scholar
  54. 54.
    Pinto JP, Ohresser MCP, Cancela ML (2001) Cloning of the Bone Gla Protein gene from the teleost fish Sparus aurata. Evidence for overall conservation in gene organization and bone-specific expression from fish to man. Gene 270:77–91PubMedCrossRefGoogle Scholar
  55. 55.
    Pinto JP, Conceição N, Gavaia PJ, Cancela ML (2003) Matrix Gla protein gene expression and protein accumulation colocalize with cartilage distribution during development of the teleost fish Sparus aurata. Bone 32:201–210PubMedCrossRefGoogle Scholar
  56. 56.
    Ferraresso S, Vitulo N, Mininni AN, Romualdi C, Cardazzo B, Negrisolo E, Reinhardt R, Canário AV, Patarnello T, Bargelloni L (2008) Development and validation of a gene expression oligo microarray for the gilthead sea bream (Sparus aurata). BMC Genomics 9:580PubMedCrossRefGoogle Scholar

Copyright information

© Springer Basel AG 2011

Authors and Affiliations

  • Marta S. Rafael
    • 1
  • Vincent Laizé
    • 1
  • Anabela Bensimon-Brito
    • 1
  • Ricardo B. Leite
    • 1
  • Roland Schüle
    • 2
  • M. Leonor Cancela
    • 1
    • 3
  1. 1.Centre of Marine Sciences (CCMAR)University of AlgarveFaroPortugal
  2. 2.Department of Urology/Women’s Hospital and Center for Clinical ResearchUniversity of Freiburg Medical CenterFreiburgGermany
  3. 3.Department of Biomedical Sciences and Medicine (DCBM)University of AlgarveFaroPortugal

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