Robert E Maxson, PhD

Title(s)Professor of Biochemistry & Molecular Medicine
SchoolKeck School of Medicine of USC
Phone+1 323 865 0633
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    The overall interest of the Maxson laboratory is the molecular genetic basis of embryonic pattern formation. We focus on processes that regulate the development of the calvaria, the flat bones that compose the top of the skull. These bones are derived from populations of neural crest and mesoderm that undergo extensive migration and proliferation as they develop into the exquisitely patterned calvarial bones. Between the bones are sutures, fibrous structures that form flexible joints uniting the bones, and that also serve as sources of stem cells that enable the bones to grow in coordination with the brain.

    Using genetic approaches in humans and mice, we have identified several genes that participate in the development of the calvarial bones and sutures. These include MSX2, which when mutated causes craniosynostosis, the fusion of the calvarial bones at the sutures, and Twist1, also required for suture development.

    Our most recent work involves an interaction between Twist1 and a related transcription factor, Tcf12. This interaction has a central role in the development of the coronal suture as well as in the pathophysiology of Saethre-Chotzen syndrome, a human disorder that results in craniosynostosis. We have investigated this interaction in mice, and in a collaboration with Gage Crump, in zebrafish. Current work focuses on how Twist1 and Tcf12 influence osteogenic precursor proliferation and differentiation, and how deficiencies in these processes lead to craniosynostosis.

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    Collapse Research Activities and Funding
    Molecular and Cellular Basis of Craniosynostosis
    NIH/NIDCR R01DE026339Jul 1, 2016 - Mar 31, 2021
    Role: Principal Investigator
    2012 Craniofacial Morphogenesis &Tissue Regeneration GRS &GRC
    NIH/NIDCR R13DE022501Feb 23, 2012 - Jun 30, 2012
    Role: Principal Investigator
    Cellular and Molecular Mechanisms of Patterned Growth of the Mammalian Skull
    NIH/NIDCR R01DE019650Apr 1, 2009 - Mar 31, 2014
    Role: Principal Investigator
    Twist1 in Boundary Formation and Craniosynostosis
    NIH/NIDCR R01DE016320Dec 1, 2004 - Aug 31, 2015
    Role: Principal Investigator
    NIH/NCRR G20RR013286Jul 15, 1999 - Jul 14, 2003
    Role: Principal Investigator
    NIH/NIDCR R01DE012450Feb 1, 1989 - Jan 31, 2008
    Role: Principal Investigator
    NIH/NICHD R01HD022416Jan 1, 1987 - Mar 31, 1997
    Role: Principal Investigator
    NIH/NICHD R01HD018582Sep 1, 1983 - Aug 31, 1998
    Role: Principal Investigator

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    Collapse Publications
    Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Researchers can login to make corrections and additions, or contact us for help.
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    1. Teng CS, Ting MC, Farmer DT, Brockop M, Maxson RE, Crump JG. Altered bone growth dynamics prefigure craniosynostosis in a zebrafish model of Saethre-Chotzen syndrome. Elife. 2018 10 25; 7. PMID: 30375332.
      View in: PubMed
    2. Nguyen BH, Ishii M, Maxson RE, Wang J. Culturing and Manipulation of O9-1 Neural Crest Cells. J Vis Exp. 2018 Oct 09; (140). PMID: 30371662.
      View in: PubMed
    3. Hughes MW, Jiang TX, Plikus MV, Guerrero-Juarez CF, Lin CH, Schafer C, Maxson R, Widelitz RB, Chuong CM. Msx2 Supports Epidermal Competency during Wound-Induced Hair Follicle Neogenesis. J Invest Dermatol. 2018 Sep; 138(9):2041-2050. PMID: 29577917.
      View in: PubMed
    4. Teng CS, Yen HY, Barske L, Smith B, Llamas J, Segil N, Go J, Sanchez-Lara PA, Maxson RE, Crump JG. Requirement for Jagged1-Notch2 signaling in patterning the bones of the mouse and human middle ear. Sci Rep. 2017 05 31; 7(1):2497. PMID: 28566723.
      View in: PubMed
    5. Sun J, Ting MC, Ishii M, Maxson R. Msx1 and Msx2 function together in the regulation of primordial germ cell migration in the mouse. Dev Biol. 2016 09 01; 417(1):11-24. PMID: 27435625.
      View in: PubMed
    6. Wang J, Xiao Y, Hsu CW, Martinez-Traverso IM, Zhang M, Bai Y, Ishii M, Maxson RE, Olson EN, Dickinson ME, Wythe JD, Martin JF. Yap and Taz play a crucial role in neural crest-derived craniofacial development. Development. 2016 Feb 01; 143(3):504-15. PMID: 26718006; PMCID: PMC4760309 [Available on 02/01/17].
    7. Liu Y, Pike MC, Wu N, Lin YG, Mucowski S, Punj V, Tang Y, Yen HY, Stanczyk FZ, Enbom E, Austria T, Widschwendter M, Maxson R, Dubeau L. Brca1 Mutations Enhance Mouse Reproductive Functions by Increasing Responsiveness to Male-Derived Scent. PLoS One. 2015; 10(10):e0139013. PMID: 26488398; PMCID: PMC4619541.
    8. Ishii M, Sun J, Ting MC, Maxson RE. The Development of the Calvarial Bones and Sutures and the Pathophysiology of Craniosynostosis. Curr Top Dev Biol. 2015; 115:131-56. PMID: 26589924.
      View in: PubMed
    9. Liu Y, Yen HY, Austria T, Pettersson J, Peti-Peterdi J, Maxson R, Widschwendter M, Dubeau L. A Mouse Model That Reproduces the Developmental Pathways and Site Specificity of the Cancers Associated With the Human BRCA1 Mutation Carrier State. EBioMedicine. 2015 Oct; 2(10):1318-30. PMID: 26629527; PMCID: PMC4634618.
    10. Cheng SL, Behrmann A, Shao JS, Ramachandran B, Krchma K, Bello Arredondo Y, Kovacs A, Mead M, Maxson R, Towler DA. Targeted reduction of vascular Msx1 and Msx2 mitigates arteriosclerotic calcification and aortic stiffness in LDLR-deficient mice fed diabetogenic diets. Diabetes. 2014 Dec; 63(12):4326-37. PMID: 25056439; PMCID: PMC4237989.
    11. Cha J, Sun X, Bartos A, Fenelon J, Lefèvre P, Daikoku T, Shaw G, Maxson R, Murphy BD, Renfree MB, Dey SK. A new role for muscle segment homeobox genes in mammalian embryonic diapause. Open Biol. 2013 Apr 24; 3(4):130035. PMID: 23615030; PMCID: PMC3718335.
    12. Yumoto K, Thomas PS, Lane J, Matsuzaki K, Inagaki M, Ninomiya-Tsuji J, Scott GJ, Ray MK, Ishii M, Maxson R, Mishina Y, Kaartinen V. TGF-ß-activated kinase 1 (Tak1) mediates agonist-induced Smad activation and linker region phosphorylation in embryonic craniofacial neural crest-derived cells. J Biol Chem. 2013 May 10; 288(19):13467-80. PMID: 23546880; PMCID: PMC3650384.
    13. Sharma VP, Fenwick AL, Brockop MS, McGowan SJ, Goos JA, Hoogeboom AJ, Brady AF, Jeelani NO, Lynch SA, Mulliken JB, Murray DJ, Phipps JM, Sweeney E, Tomkins SE, Wilson LC, Bennett S, Cornall RJ, Broxholme J, Kanapin A, Johnson D, Wall SA, van der Spek PJ, Mathijssen IM, Maxson RE, Twigg SR, Wilkie AO. Mutations in TCF12, encoding a basic helix-loop-helix partner of TWIST1, are a frequent cause of coronal craniosynostosis. Nat Genet. 2013 Mar; 45(3):304-7. PMID: 23354436.
      View in: PubMed
    14. Sun J, Ishii M, Ting MC, Maxson R. Foxc1 controls the growth of the murine frontal bone rudiment by direct regulation of a Bmp response threshold of Msx2. Development. 2013 Mar; 140(5):1034-44. PMID: 23344708; PMCID: PMC3583041.
    15. Ishii M, Arias AC, Liu L, Chen YB, Bronner ME, Maxson RE. A stable cranial neural crest cell line from mouse. Stem Cells Dev. 2012 Nov 20; 21(17):3069-80. PMID: 22889333; PMCID: PMC3495126.
    16. Yen HY, Gabet Y, Liu Y, Martin A, Wu NL, Pike MC, Frenkel B, Maxson R, Dubeau L. Alterations in Brca1 expression in mouse ovarian granulosa cells have short-term and long-term consequences on estrogen-responsive organs. Lab Invest. 2012 Jun; 92(6):802-11. PMID: 22488153; PMCID: PMC4530993.
    17. Ting MC, Liao CP, Yan C, Jia L, Groshen S, Frenkel B, Roy-Burman P, Coetzee GA, Maxson R. An enhancer from the 8q24 prostate cancer risk region is sufficient to direct reporter gene expression to a subset of prostate stem-like epithelial cells in transgenic mice. Dis Model Mech. 2012 May; 5(3):366-74. PMID: 22279083; PMCID: PMC3339830.
    18. Daikoku T, Cha J, Sun X, Tranguch S, Xie H, Fujita T, Hirota Y, Lydon J, DeMayo F, Maxson R, Dey SK. Conditional deletion of Msx homeobox genes in the uterus inhibits blastocyst implantation by altering uterine receptivity. Dev Cell. 2011 Dec 13; 21(6):1014-25. PMID: 22100262; PMCID: PMC3241866.
    19. Yen HY, Ting MC, Maxson RE. Jagged1 functions downstream of Twist1 in the specification of the coronal suture and the formation of a boundary between osteogenic and non-osteogenic cells. Dev Biol. 2010 Nov 15; 347(2):258-70. PMID: 20727876; PMCID: PMC3210079.
    20. Roybal PG, Wu NL, Sun J, Ting MC, Schafer CA, Maxson RE. Inactivation of Msx1 and Msx2 in neural crest reveals an unexpected role in suppressing heterotopic bone formation in the head. Dev Biol. 2010 Jul 01; 343(1-2):28-39. PMID: 20398647; PMCID: PMC3279331.
    21. Pace DA, Maxson R, Manahan DT. Ribosomal analysis of rapid rates of protein synthesis in the Antarctic sea urchin Sterechinus neumayeri. Biol Bull. 2010 Feb; 218(1):48-60. PMID: 20203253.
      View in: PubMed
    22. Hong H, Yen HY, Brockmeyer A, Liu Y, Chodankar R, Pike MC, Stanczyk FZ, Maxson R, Dubeau L. Changes in the mouse estrus cycle in response to BRCA1 inactivation suggest a potential link between risk factors for familial and sporadic ovarian cancer. Cancer Res. 2010 Jan 01; 70(1):221-8. PMID: 20028858; PMCID: PMC2805040.
    23. Ting MC, Wu NL, Roybal PG, Sun J, Liu L, Yen Y, Maxson RE. EphA4 as an effector of Twist1 in the guidance of osteogenic precursor cells during calvarial bone growth and in craniosynostosis. Development. 2009 Mar; 136(5):855-64. PMID: 19201948; PMCID: PMC2685950.
    24. Asahina K, Tsai SY, Li P, Ishii M, Maxson RE, Sucov HM, Tsukamoto H. Mesenchymal origin of hepatic stellate cells, submesothelial cells, and perivascular mesenchymal cells during mouse liver development. Hepatology. 2009 Mar; 49(3):998-1011. PMID: 19085956; PMCID: PMC2673117.
    25. Plikus MV, Widelitz RB, Maxson R, Chuong CM. Analyses of regenerative wave patterns in adult hair follicle populations reveal macro-environmental regulation of stem cell activity. Int J Dev Biol. 2009; 53(5-6):857-68. PMID: 19378257; PMCID: PMC2759942.
    26. Li P, Tong C, Mehrian-Shai R, Jia L, Wu N, Yan Y, Maxson RE, Schulze EN, Song H, Hsieh CL, Pera MF, Ying QL. Germline competent embryonic stem cells derived from rat blastocysts. Cell. 2008 Dec 26; 135(7):1299-310. PMID: 19109898; PMCID: PMC2735113.
    27. Chen YH, Ishii M, Sucov HM, Maxson RE. Msx1 and Msx2 are required for endothelial-mesenchymal transformation of the atrioventricular cushions and patterning of the atrioventricular myocardium. BMC Dev Biol. 2008 Jul 30; 8:75. PMID: 18667074; PMCID: PMC2518925.
    28. Plikus MV, Mayer JA, de la Cruz D, Baker RE, Maini PK, Maxson R, Chuong CM. Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature. 2008 Jan 17; 451(7176):340-4. PMID: 18202659; PMCID: PMC2696201.
    29. Maxson R, Ishii M. The Bmp pathway in skull vault development. Front Oral Biol. 2008; 12:197-208. PMID: 18391502.
      View in: PubMed
    30. Fu H, Ishii M, Gu Y, Maxson R. Conditional alleles of Msx1 and Msx2. Genesis. 2007 Aug; 45(8):477-81. PMID: 17654563.
      View in: PubMed
    31. Han J, Ishii M, Bringas P, Maas RL, Maxson RE, Chai Y. Concerted action of Msx1 and Msx2 in regulating cranial neural crest cell differentiation during frontal bone development. Mech Dev. 2007 Sep-Oct; 124(9-10):729-45. PMID: 17693062; PMCID: PMC2220014.
    32. Chen YH, Ishii M, Sun J, Sucov HM, Maxson RE. Msx1 and Msx2 regulate survival of secondary heart field precursors and post-migratory proliferation of cardiac neural crest in the outflow tract. Dev Biol. 2007 Aug 15; 308(2):421-37. PMID: 17601530.
      View in: PubMed
    33. Chai Y, Maxson RE. Recent advances in craniofacial morphogenesis. Dev Dyn. 2006 Sep; 235(9):2353-75. PMID: 16680722.
      View in: PubMed
    34. Merrill AE, Bochukova EG, Brugger SM, Ishii M, Pilz DT, Wall SA, Lyons KM, Wilkie AO, Maxson RE. Cell mixing at a neural crest-mesoderm boundary and deficient ephrin-Eph signaling in the pathogenesis of craniosynostosis. Hum Mol Genet. 2006 Apr 15; 15(8):1319-28. PMID: 16540516.
      View in: PubMed
    35. Ishii M, Han J, Yen HY, Sucov HM, Chai Y, Maxson RE. Combined deficiencies of Msx1 and Msx2 cause impaired patterning and survival of the cranial neural crest. Development. 2005 Nov; 132(22):4937-50. PMID: 16221730.
      View in: PubMed
    36. Liu W, Selever J, Murali D, Sun X, Brugger SM, Ma L, Schwartz RJ, Maxson R, Furuta Y, Martin JF. Threshold-specific requirements for Bmp4 in mandibular development. Dev Biol. 2005 Jul 15; 283(2):282-93. PMID: 15936012.
      View in: PubMed
    37. Maxson R. Adaptation: a developmental biologist in the Antarctic. Genesis. 2005 Jul; 42(3):117-23. PMID: 15986441.
      View in: PubMed
    38. Chodankar R, Kwang S, Sangiorgi F, Hong H, Yen HY, Deng C, Pike MC, Shuler CF, Maxson R, Dubeau L. Cell-nonautonomous induction of ovarian and uterine serous cystadenomas in mice lacking a functional Brca1 in ovarian granulosa cells. Curr Biol. 2005 Mar 29; 15(6):561-5. PMID: 15797026.
      View in: PubMed
    39. Brugger SM, Merrill AE, Torres-Vazquez J, Wu N, Ting MC, Cho JY, Dobias SL, Yi SE, Lyons K, Bell JR, Arora K, Warrior R, Maxson R. A phylogenetically conserved cis-regulatory module in the Msx2 promoter is sufficient for BMP-dependent transcription in murine and Drosophila embryos. Development. 2004 Oct; 131(20):5153-65. PMID: 15459107.
      View in: PubMed
    40. Ishii M, Merrill AE, Chan YS, Gitelman I, Rice DP, Sucov HM, Maxson RE. Msx2 and Twist cooperatively control the development of the neural crest-derived skeletogenic mesenchyme of the murine skull vault. Development. 2003 Dec; 130(24):6131-42. PMID: 14597577.
      View in: PubMed
    41. Wu LY, Li M, Hinton DR, Guo L, Jiang S, Wang JT, Zeng A, Xie JB, Snead M, Shuler C, Maxson RE, Liu YH. Microphthalmia resulting from MSX2-induced apoptosis in the optic vesicle. Invest Ophthalmol Vis Sci. 2003 Jun; 44(6):2404-12. PMID: 12766037.
      View in: PubMed
    42. Ma L, Liu J, Wu T, Plikus M, Jiang TX, Bi Q, Liu YH, Müller-Röver S, Peters H, Sundberg JP, Maxson R, Maas RL, Chuong CM. 'Cyclic alopecia' in Msx2 mutants: defects in hair cycling and hair shaft differentiation. Development. 2003 Jan; 130(2):379-89. PMID: 12466204; PMCID: PMC4386654.
    43. Jiang X, Choudhary B, Merki E, Chien KR, Maxson RE, Sucov HM. Normal fate and altered function of the cardiac neural crest cell lineage in retinoic acid receptor mutant embryos. Mech Dev. 2002 Sep; 117(1-2):115-22. PMID: 12204252.
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    44. Kwang SJ, Brugger SM, Lazik A, Merrill AE, Wu LY, Liu YH, Ishii M, Sangiorgi FO, Rauchman M, Sucov HM, Maas RL, Maxson RE. Msx2 is an immediate downstream effector of Pax3 in the development of the murine cardiac neural crest. Development. 2002 Jan; 129(2):527-38. PMID: 11807043.
      View in: PubMed
    45. Jiang X, Iseki S, Maxson RE, Sucov HM, Morriss-Kay GM. Tissue origins and interactions in the mammalian skull vault. Dev Biol. 2002 Jan 01; 241(1):106-16. PMID: 11784098.
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