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          Labs @ NIAMS
          Laboratory of Skin Biology








Laboratory of Skin Biology


Maria I. Morasso, Ph.D. FacebookEmailPrintFacebookEmail
        Assembly of 4 images from research publications

      Overview

                                  Senior Investigator
      
  


Maria I. Morasso, Ph.D.
      
  


            morassom@mail.nih.gov
      
                                                                        

  
   Research Areas (IRP Lab Groups)
          Cancer Biology,
          Developmental Biology,
          Genetics and Genomics,
          Molecular Biology and Biochemistry,
          Skin Biology
                                
            The pathways that regulate epidermal differentiation and the formation of a functional skin barrier have been a central topic of investigation in epidermal biology. Our research efforts have focused on characterizing the transcriptional regulatory networks and signaling pathways linked to epidermal differentiation and wound healing.

Epidermal Differentiation and Inflammatory Disorders

Epidermal homeostasis results from a balance between keratinocyte proliferation and differentiation, with alterations to this balance leading to cancer. Using animal models, we have demonstrated the central role of the transcriptional regulator during epidermal differentiation. Through a combination of transcriptomic and bioinformatic analyses, we have identified a DLX3-dependent network that regulates cell cycle and the activated ERK- and STAT3-dependent signaling pathways that are crucial to maintaining cutaneous homeostasis. The epidermal conditional deletion of DLX3 leads to the disruption of skin barrier formation. It is linked to epidermal hyperplasia and the development of an inflammatory response, characterized by the accumulation of IL-17-producing T cells. Our studies also provide a novel understanding of the signaling networks regulating squamous tumorigenesis.

Wound Healing
Illustrated cross-section of inflamed, normal and wounded skin.Schematic diagram showing epidermal differentiation, inflammation and wounding.Oral wounds are considered an ideal prototype of adult tissue repair due to their intrinsic ability for scarless accelerated wound healing. Our studies have shown that wound-activated transcriptional networks are active in oral mucosa at a basal state, priming this tissue for wound repair by controlling epithelial cell differentiation. We have determined the capability of the SOX2 and PITX1 transcription factors to reprogram cutaneous keratinocytes for accelerated wound resolution. Furthermore, we found that SOX2 promotes keratinocyte migration and angiogenesis through the upregulation of EGFR ligands and activation of the ERK/MAPK pathway. In contrast to acute cutaneous and oral wounds, chronic non-healing wounds do not resolve and are characterized by deregulated inflammation. This is due to ineffective recruitment and activation of macrophages and neutrophils. We are currently focused on identifying pathways responsible for the downregulation of inflammation that will be pivotal for diagnostics and the development of potential therapeutics.

Ectodermal Dysplasias and Ectodermal Appendage Development

Ectodermal dysplasias are a group of heritable pathological disorders that result from anomalies in epithelial/mesenchymal-derived appendage formation. The importance of DLX3 is underscored by the effects of mutations found in patients with autosomal dominant Tricho-Dento-Osseous (TDO) syndrome. We have demonstrated the crucial role of DLX3 in epidermal development and tooth and hair formation through direct regulation of specific sets of keratins. Using genetic and intraoral examination data from human patients, we identified several missense polymorphisms in keratins that lead to a higher risk for dental caries.
      

                                            Scientific Advances
      
  

      July 28, 2023Upregulation of the Protein Amphiregulin Protects Against Pressure Ulcers
    July 13, 2023Role of Neurotrophin Receptor CD271 in Cutaneous Squamous Cell Carcinoma Invasiveness Identified
    July 1, 2023Epigenomic Landscape of Murine Skin Epidermis Differentiation Revealed
    July 20, 2022Neutrophil Function in Diabetic Foot Ulcers

                                                      Core Research Facilities

Labs at the NIAMS are supported by the following state-of-the-art facilities and services:

Biodata Mining and Discovery
	Flow Cytometry
	Genomic Technology
	Laboratory Animal Care and Use
	Light Imaging
	Translational Immunology

                                    Staff
                            
            **Maria I. Morasso, Ph.D.**Senior Investigatormorassom@mail.nih.gov
    **Kowser Hasneen, B.S., M.S.**Biologistkowser.hasneen@nih.gov
    **Subhashree Nayak, Ph.D.**Research Fellownayaks2@mail.nih.gov
    **Andrew Overmiller, Ph.D.**Postdoctoral Fellowandrew.overmiller@nih.gov
    **Christopher O’Neill, B.A.**Postbaccalaureate Fellowoneillcg@nih.gov
      

              
                            Former Lab Members
              Postdoctoral FellowsDaniela Grassini, Visiting Fellow (2018-2021)Akihiko Uchiyama, Visiting Fellow, JSPS Fellowship (2016-2019)Shreya Bhattacharya, Visiting Fellow (2014-2017)Kathleen Baysac, IRTA Fellow (2015-2017)Ramiro Iglesias-Bartolome, Research Fellow (2015-2016)Paul Bible, IRTA Fellow (2013-2015)Jin-Chul Kim, Visiting Fellow (2010-2015)Juliane Lessard, IRTA Fellow (2013-2014)Elisabetta Palazzo, Visiting Fellow (2011-2014)Juliane Isaac, Visiting Fellow (2009-2013)Junko Okano, Visiting Fellow (2008-2012)Olivier Duverger, Visiting Fellow (2006-2011)Joonsung Hwang, Visiting Fellow (2004-2011)Oleksandr Kalinin, Visiting Fellow (2004-2008)Valentina Pietroni, Visiting Fellow (2006-2008)Nadezda Radoja, IRTA Fellow (2004-2006)Meeyul Hwang, Visiting Fellow (2001-2005)Janine Bryan, IRTA Fellow (2000-2002)Geon Tae Park, Visiting Fellow (2000-2003)Postbaccalaureate FellowsEmma Hope (2020-2022)Stephen Worrell (2020-2021)Michael Cross (2017-2019)Rose Graf (2017-2018)Veronica Nagle (2016-2017)Maya Evanitsky (2016-2017)Chelsea Karacz (2015-2017)Meghan Kellett (2013-2016)Victoria Sun (2014-2015)Takahiro O'Hara (2012-2014)Anna Gormley (2012-2013)Claire Levy (2011-2012)Angela Zah (2010-2012)Anne Bartels (2009-2010)Ryosuke Kita (2009-2010)Nicole Gentile (2007-2008)Susie Chen (2007-2008)Delia Lee (2006-2007)Sarah-Jo Stimpson (2005-2006)Charlene Rivera (2001-2002)Taraneh Mehrani (2000-2001)Research FellowsDeepti Bajpai, Research Fellow (2017-2022)Staff ScientistOlivier Duverger, Staff Scientist (2011-2017)
            
                                                Image & Media Gallery
              
            Human Buccal Mucosa Section
Human Buccal Mucosa Section
        ×
      Human Buccal Mucosa Section
        Human buccal mucosa section (5μm) immunostained for fibroblasts with vimentin (green), keratinocytes with keratin 5 (magenta), and nuclei with DAPI (blue). Slide imaged (20X) on Leica TC SP8 X confocal microscope (Light Imaging Section, NIH/NIAMS).
    Human Buccal Mucosa Section
Human Buccal Mucosa Section
        ×
      Human Buccal Mucosa Section
        Human buccal mucosa section (5μm) immunostained for fibroblasts with vimentin (green) and keratinocytes with keratin 5 (magenta). Slide imaged (20X) on Leica TC SP8 X confocal microscope (Light Imaging Section, NIH/NIAMS).
    Human Buccal Mucosa Section
Human Buccal Mucosa Section
        ×
      Human Buccal Mucosa Section
        Human buccal mucosa section (5μm) immunostained for fibroblasts with vimentin (green) and nuclei with DAPI (blue). Slide imaged (20X) on Leica TC SP8 X confocal microscope (Light Imaging Section, NIH/NIAMS).
    The Morasso Lab (2020)
The Morasso Lab (2020)
        ×
      Video conference call with lab members arranged in a grid.
        Weekly Lab meeting - video conference call.

Top row: Subhashree Nayak; Emma Hope; Kowser Hasneen
Middle row: Stephen Worrell; Daniela Grassini; Andrew Sawaya
Bottom row: Deepti Bajpai; Spencer Mehdizadeh; Andrew Overmiller
Bottom small photo: Maria I. Morasso
    Immunofluoresecence of SAOS cells
Immunofluoresecence of SAOS cells
        ×
      Immunofluoresecence of SAOS cells
        Immunofluoresecence of SAOS cells expressing GFP (teal) counterstained with DAPI (magenta)

*Olivier Duverger and Maria Morasso, Laboratory of Skin Biology*
(Image acquired using Zeiss LSM780 confocal microscope)
         Download High Res
    (412.09 KB)
    Mouse Papilloma
Mouse Papilloma
        ×
      Immunofluorescence of mouse papilloma section
        Immunofluorescence of mouse papilloma section detecting PCNA (red), CD45 (green), KRT5 (orange) and nuclei counterstained with Dapi (blue).

*Deepti Bajpai and Spencer Mehdizadeh, Laboratory of Skin Biology*
(Image acquired using laser-scanning confocal microscope Zeiss LSM780)
         Download High Res
    (690.01 KB)
    Vascular Tree
Vascular Tree
        ×
      Whole-mount, fluorescence immunohistochemistry of mouse back skin
        Whole-mount, fluorescence immunohistochemistry of mouse back skin. Blood vessels labelled with an anti-CD31 (PECAM-1, Platelet and Endothelial Cell Adhesion Molecule 1) antibody (grey), vSMCs (vascular Smooth Muscle Cells) labelled with an anti-aSMA (alpha Smooth Muscle Actin) antibody (green), and the extracellular matrix surrounding the vessels is stained with an anti-Collagen 4a4 antibody (green).

*Daniela Grassini, Laboratory of Skin Biology*
(captured with Zeiss LSM780 confocal microscope)
         Download High Res
    (1.08 MB)
    Planetoid
Planetoid
        ×
      Planetoid
        Immunofluorescence of cutaneous squamous cell carcinoma tumor core for suprabasin (green), keratin 14 (red) and nuclei with DAPI (blue).

*Andrew Overmiller, Laboratory of Skin Biology*
(image acquired on a Leica SP8 confocal microscope)
    Primary Human Keratinocytes in 3D
Primary Human Keratinocytes in 3D
        ×
      Primary Human Keratinocytes in 3D
        Super-resolution imaging of primary human keratinocytes detecting keratin 75 (green), the inner nuclear membrane protein SUN2 (red) and the transcription factor SOX2 (purple).

*Andrew Sawaya, Laboratory of Skin Biology*
(Image acquired on a Leica TCS SP8 X confocal microscope)
         Download High Res
    (1.69 MB)
    Immunocytochemistry of ameloblast-like cells
Immunocytochemistry of ameloblast-like cells
        ×
      Immunocytochemistry of ameloblast-like cells
        Immunocytochemistry of ameloblast-like cells transfected to overexpress a mutant form of keratin 6 (red) associated with dental cavities. Counterstained with phalloidin (white) and Dapi (blue).

*Olivier Duverger and Michael Cross, Laboratory of Skin Biology*
(captured with Zeiss LSM780 confocal microscope)
    Immunohistochemistry of Oral Buccal Mucosa
Immunohistochemistry of Oral Buccal Mucosa
        ×
      Immunohistochemistry of Oral Buccal Mucosa
        Immunohistochemistry of oral buccal mucosa detecting Annexin 1 (magenta), Keratin 5 (red) and SLPI (green)

*Ramiro Iglesias-Bartolome and Maria Morasso, Laboratory of Skin Biology*
(captured with: Zeiss LSM780 confocal microscope)
         Download High Res
    (5.86 MB)
    Morasso Lab Group Photo
Morasso Lab Group Photo
        ×
      Morasso Lab group photo
        
         Download High Res
    (310.98 KB)
    Cover for Science Translational Medicine (July 25, 2018)
Cover for Science Translational Medicine (July 25, 2018)
        ×
      Cover of Science Translational Medicine - July 25, 2018
        Hastened Healing. Wounds in the human mouth, such as this biopsy taken from injured oral mucosa and stained for the epithelial markers keratin 6 (green) and keratin 5 (red), heal faster than wounds in other locations on the body. Iglesias-Bartolome *et al*. used transcriptomics to study differences in gene expression during wound healing, using paired oral and skin biopsies from healthy human subjects. They found several transcription factors that were up-regulated in oral mucosa compared to skin. Overexpressing one of these factors in a mouse model of skin wounding improved healing. These findings could eventually help inform targeted therapy design for wound healing. [CREDIT: IGLESIAS-BARTOLOME *ET AL.*/*SCIENCE TRANSLATIONAL MEDICINE*]

Cover from Science Translational Medicine, July 25, 2018.
    Altered skin differentiation in Cyp26b1−/− epidermis
Altered skin differentiation in Cyp26b1−/− epidermis
        ×
      Laboratory of Skin Biology Figure 1
        Pan-Krt; pan-keratin (red) and involucrin (Inv; green) were detected by immunohistochemistry in E18.5 Cyp26b1−/− skin. DAPI staining is blue.

Images were acquired using a Zeiss 510 Meta confocal microscope.

Publication: Okano et al. *J Cell Sci*. (2012) 125(7): 1827–1836.
PubMed: 22366455
    Dlx3 expression during craniofacial development
Dlx3 expression during craniofacial development
        ×
      Laboratory of Skin Biology Figure 2
        LacZ staining in the calvaria (top view of the head) of Dlx3LacZ/WT mice at E16.5.
Publication: Duverger et al. J Cell Physiol. (2013) 228(3): 654–664.

Images were acquired using an Olympus SZX9 dissecting microscope.
    Deletion of Dlx3 in the dental mesenchyme using Wnt1-cre mice.
Deletion of Dlx3 in the dental mesenchyme using Wnt1-cre mice.
        ×
      Laboratory of Skin Biology Figure 4
        Dlx3 expression on mandibular molars (coronal section) from Wnt1-cre:R26RYFP at E14.5 YFP, green; Dlx3, red; DAPI, blue.
Publication: Duverger et al. J Biological Chem. (2012) 287(15): 12230-12240.
    Histological analysis of Dlx3 expression in patient samples (psoriasis and atopic dermatitis).
Histological analysis of Dlx3 expression in patient samples (psoriasis and atopic dermatitis).
        ×
      Laboratory of Skin Biology Figure 5
        Dlx3 expression (green), keratin 5 (K5, red) and DAPI (blue) counterstaining to denote nuclear staining. 
Publication: Hwang et al. (2011) PNAS 108 (28): 11566-11571
    FASEB BioArt winner 2015
FASEB BioArt winner 2015
        ×
      Laboratory of Skin Biology Figure 6
        Scanning-electron-microscopy image shows the lattice pattern formed by enamel rods.

Publication: Duverger er al. J Clin Invest. (2014) 124(12):5219-24.

https://irp.nih.gov/catalyst/v24i1/photographic-moment

https://irp.nih.gov/blog/post/2016/03/snapshots-of-life-stronger-than-it-looks
    Whole mount staining of mouse skin from Wnt1-cre:RosaYFP neonate
Whole mount staining of mouse skin from Wnt1-cre:RosaYFP neonate
        ×
      Laboratory of Skin Biology Figure 9
        Whole mount staining of mouse skin from Wnt1-cre:RosaYFP neonate with Phalloidin-Alexa 568 (actin filament in red) and DAPI (blue). YFP (green) marks neural crest-derived cells in the developing hair follicles. Image acquired on a Leica SP5 confocal microscope. (from Olivier Duverger; Morasso Lab).
    Immunohistochemical detection of the epithelial keratins
Immunohistochemical detection of the epithelial keratins
        ×
      Laboratory of Skin Biology Figure 10
        **Immunohistochemical detection of the epithelial keratins (green and red) in the enamel organ from mouse mandibular incisor at post-natal day 2.** DAPI (blue) was used to mark the nuclei. Image acquired on a Leica SP5 confocal microscope. (from Olivier Duverger; Morasso Lab).
    Ameloblast-like cell line (ALCs) overexpressing mutant form of keratin-6a.
Ameloblast-like cell line (ALCs) overexpressing mutant form of keratin-6a.
        ×
      Laboratory of Skin Biology Figure 11
        **Ameloblast-like cell line (ALCs) overexpressing mutant form of keratin-6a.**

Cells were stained with anti-K6 (red), DAPI (blue), and phalloidin (white).

(Image Credit: Michael Cross; Morasso lab)
            
                        
                        
                                    Scientific Publications
              Selected Recent Publications
                  
      Keratin 75 Is a Component of the LINC Complex and Has an Essential Role in Mediating the SOX2 Rapid Healing Response during Wound Repair.

    Sawaya AP, Uchiyama A, Hope E, Bajpai D, Worrell S, Cross M, Beniash E, Jenkins LM, Duverger O, Morasso MI
        

                    J Invest Dermatol.
        
                    2023 Mar;
        
                    143(3).
        
                    doi: 10.1016/j.jid.2022.08.054
                            PMID: 36174715
              Intrinsic Networks Regulating Tissue Repair: Comparative Studies of Oral and Skin Wound Healing.

    Overmiller AM, Sawaya AP, Hope ED, Morasso MI
        

                    Cold Spring Harb Perspect Biol.
        
                    2022 Nov 1;
        
                    14(11).
        
                    doi: 10.1101/cshperspect.a041244
                            PMID: 36041785
              Transcriptional Regulation of Jaw Osteoblasts: Development to Pathology.

    Nassif A, Lignon G, Asselin A, Zadikian CC, Petit S, Sun HW, Klein C, Ferré FC, Morasso MI, Berdal A, Fournier BPJ, Isaac J
        

                    J Dent Res.
        
                    2022 Jul;
        
                    101(7).
        
                    doi: 10.1177/00220345221074356
                            PMID: 35148649
              SOX2 Epidermal Overexpression Promotes Cutaneous Wound Healing via Activation of EGFR/MEK/ERK Signaling Mediated by EGFR Ligands.

    Uchiyama A, Nayak S, Graf R, Cross M, Hasneen K, Gutkind JS, Brooks SR, Morasso MI
        

                    J Invest Dermatol.
        
                    2019 Aug;
        
                    139(8).
        
                    doi: 10.1016/j.jid.2019.02.004
                            PMID: 30772301
              Ectodermal dysplasias: Classification and organization by phenotype, genotype and molecular pathway.

    Wright JT, Fete M, Schneider H, Zinser M, Koster MI, Clarke AJ, Hadj-Rabia S, Tadini G, Pagnan N, Visinoni AF, Bergendal B, Abbott B, Fete T, Stanford C, Butcher C, D'Souza RN, Sybert VP, Morasso MI
        

                    Am J Med Genet A.
        
                    2019 Mar;
        
                    179(3).
        
                    doi: 10.1002/ajmg.a.61045
                            PMID: 30703280
              DLX3-Dependent STAT3 Signaling in Keratinocytes Regulates Skin Immune Homeostasis.

    Bhattacharya S, Kim JC, Ogawa Y, Nakato G, Nagle V, Brooks SR, Udey MC, Morasso MI
        

                    J Invest Dermatol.
        
                    2018 May;
        
                    138(5).
        
                    doi: 10.1016/j.jid.2017.11.033
                            PMID: 29246798
              Genetic variants in pachyonychia congenita-associated keratins increase susceptibility to tooth decay.

    Duverger O, Carlson JC, Karacz CM, Schwartz ME, Cross MA, Marazita ML, Shaffer JR, Morasso MI
        

                    PLoS Genet.
        
                    2018 Jan;
        
                    14(1).
        
                    doi: 10.1371/journal.pgen.1007168
                            PMID: 29357356
              A novel DLX3-PKC integrated signaling network drives keratinocyte differentiation.

    Palazzo E, Kellett MD, Cataisson C, Bible PW, Bhattacharya S, Sun HW, Gormley AC, Yuspa SH, Morasso MI
        

                    Cell Death Differ.
        
                    2017 Apr;
        
                    24(4).
        
                    doi: 10.1038/cdd.2017.5
                            PMID: 28186503
                
                                Key Publications
                  
            Chromatin Landscape Governing Murine Epidermal Differentiation.Nayak S, Jiang K, Hope E, Cross M, Overmiller A, Naz F, Worrell S, Bajpai D, Hasneen K, Brooks SR, Dell'Orso S, Morasso MIJ Invest Dermatol.2023 Jul;143(7).doi: 10.1016/j.jid.2022.12.020PMID: 36708949Scientific AdvanceFOXM1 network in association with TREM1 suppression regulates NET formation in diabetic foot ulcers.Sawaya AP, Stone RC, Mehdizadeh S, Pastar I, Worrell S, Balukoff NC, Kaplan MJ, Tomic-Canic M, Morasso MIEMBO Rep.2022 Aug 3;23(8).doi: 10.15252/embr.202154558PMID: 35856334Scientific AdvanceHuman oral mucosa cell atlas reveals a stromal-neutrophil axis regulating tissue immunity.Williams DW, Greenwell-Wild T, Brenchley L, Dutzan N, Overmiller A, Sawaya AP, Webb S, Martin D, NIDCD/NIDCR Genomics and Computational BiologyCell.2021 Jul 22;184(15).doi: 10.1016/j.cell.2021.05.013PMID: 34129837Loss of DLX3 tumor suppressive function promotes progression of SCC through EGFR-ERBB2 pathway.Bajpai D, Mehdizadeh S, Uchiyama A, Inoue Y, Sawaya A, Overmiller A, Brooks SR, Hasneen K, Kellett M, Palazzo E, Motegi SI, Yuspa SH, Cataisson C,Oncogene.2021 May;40(21).doi: 10.1038/s41388-021-01802-9PMID: 33947961Deregulated immune cell recruitment orchestrated by FOXM1 impairs human diabetic wound healing.Sawaya AP, Stone RC, Brooks SR, Pastar I, Jozic I, Hasneen K, O'Neill K, Mehdizadeh S, Head CR, Strbo N, Morasso MI, Tomic-Canic MNat Commun.2020 Sep 16;11(1).doi: 10.1038/s41467-020-18276-0PMID: 32938916Data and AnalysisTranscriptional signature primes human oral mucosa for rapid wound healing.Iglesias-Bartolome R, Uchiyama A, Molinolo AA, Abusleme L, Brooks SR, Callejas-Valera JL, Edwards D, Doci C, Asselin-Labat ML, Onaitis MW,Sci Transl Med.2018 Jul 25;10(451).pii: eaap8798. doi: 10.1126/scitranslmed.aap8798PMID: 30045979Data and AnalysisHair keratin mutations in tooth enamel increase dental decay risk.Duverger O, Ohara T, Shaffer JR, Donahue D, Zerfas P, Dullnig A, Crecelius C, Beniash E, Marazita ML, Morasso MIJ Clin Invest.2014 Dec;124(12).doi: 10.1172/JCI78272PMID: 25347471 
                            See all Publications on PubMed
            
                                    News & Highlights
              
            NIH News in Health | October 2, 2023
To Heal a Wound: Helping the Skin Fix Itself
Wounds that don’t heal for three months or more are called chronic wounds. Your risk for getting a chronic wound increases with age. But there are ways you can help your body to heal.
Read More
    NIAMS-Related Article | September 15, 2022
Overzealous Immune Cells Hamper Healing
For a type of wound that often plagues patients with diabetes, healing is no sure thing. IRP researchers recently identified why certain immune cells shift from helpful healers into saboteurs in those injuries.
Read More
    NIAMS-Related Article | October 27, 2021
The mouth’s curative superpowers
Wounds in the mouth heal faster than in skin — and without scarring. Could unravelling the mechanisms that drive regeneration in the oral cavity lead to better wound therapies?
Read More
    Spotlight on Research | November 2, 2020
Researchers Uncover Clues to Why Some Wounds Don’t Heal
Researchers identify defects in the wound healing process that might explain why diabetic foot ulcers heal slower or not at all.
Read More
    NIH Research Matters | September 29, 2020
Poor immune response impairs diabetic wound healing
Researchers found that diabetic foot ulcers don’t recruit the immune cells necessary for normal wound healing.
Read More
    YouTube Video | July 25, 2018
NIH Study Examines Processes Underlying Rapid Wound Healing in the Mouth
Researchers from the NIH’s NIAMS and the NIDCR have identified transcriptional regulators that prime the mouth’s
Read More



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        Last Updated: November 2023
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