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MIOFIBROBLASTOS, CLULAS RELEVANTES NASADE E NA DOENA: REVISES DELITERATURA

ARTICLE NOVEMBER 2014

DOI: 10.17267/2238-2720revbahianaodonto.v5i2.416

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Bahiana School of Medicine and Public Hea

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REVISES DE LITERATURA

MIOFIBROBLASTOSCLULAS RELEVANTES NA SADE

E NA DOENArevises de literatura

Flvia Godinho Costa Wanderley a

Slvia Regina de Almeida Reis b

Alena Ribeiro Alves Peixoto Medrado c

Resumo

Recentemente, um grande nmero de estudos sobre miofibroblastos tem sido publicados. Estes ele-

mentos celulares foram primariamente descritos h mais de 40 anos e as suas caractersticas ul-

traestruturais, assim como seu papel em diversas condies fisiolgicas e patolgicas continuam

despertando interesse nas reas de sade. O presente trabalho objetiva descrever a biologia celular e

molecular dos miofibroblastos, contextualizando as descobertas cientficas sobre estas clulas regis-

tradas em artigos ao longo dos ltimos 40 anos desde a sua descoberta inicial.

Palavras-chave: Mofibroblastos; Tecido conjuntivo; Patologia.

MYOFIBROBLASTS - IMPORTANT CELLS IN HEALTH

AND DISEASE

Abstract

Recently, a large number of studies about myofibroblasts have been published. These cellular elements

were primarily described for over 40 years and their ultrastructural characteristics, as well as its role in

various physiological and pathological conditions continue stirring interest in health area. This paper

Autor correspondente: Alena Peixoto Medrado - [email protected]

a. Estudante de Iniciao Cientfica da Escola Bahiana de Medicina e Sade Pblica, Salvador, Bahia, Brasil. BolsistaFapesb

b. Doutora em Patologia Oral pela Universidade Livre de Berlim. Professora adjunta do curso de Odontologia da EscolaBahiana de Medicina e Sade Pblica, Salvador, Bahia, Brasil

c. Doutora em Patologia Humana pela Fiocruz/UFBA, professora adjunta da Escola Bahiana de Medicina e Sade Pblica,Salvador, Bahia, Brasil

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Revista Bahiana de Odontologia. 2014 Ago;5(2):117-124

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aims to describe the cellular and molecular biology of myofibroblasts, and contextualize scientific findings of

these cells recorded in articles over the past 40 years since its initial discovery.

Keywords: Myofibroblasts; Connective tissue; Pathology.

INTRODUO

O miofibroblasto foi descoberto em eletromicro-

grafias de tecido de granulao presente em pro-

cessos de cicatrizao induzidos experimental-

mente.(1)

Logo depois, suas caractersticas bioqumicas e

imunolgicas passaram a ser amplamente estuda-

das. A partir destas descobertas, a lista de condi-

es patolgicas nas quais estas clulas tm sido

identificadas, tem crescido consideravelmente. Du-

rante muitos anos, a distribuio espacial de tais

clulas em carcinomas metastticos foi descrita

por Gabbiani,(2)e foi proposto que havia similari-

dades entre o processo de cicatrizao tecidual ea resposta do estroma invaso metasttica. Nos

anos seguintes, foram realizados detalhados es-

tudos a respeito dos filamentos intermedirios e

isoformas de actina presentes em miofibroblastos

sob diversas circunstncias. Outras investigaes

demonstraram que existe uma correlao entre a

modulao fenotpica do citoesqueleto de miofi-

broblastos e o comportamento clnico das leses

que contm estas clulas. Em particular, foi obser-

vado que os miofibroblastos em tecido de granula-

o presentes em feridas cicatriciais expressam o

fentipo de msculo liso apenas temporariamente,

embora miofibroblastos com um fentipo de

msculo liso persistam em cicatrizes anormais,

doenas fibrocontrteis e condies proliferativas

neoplsicas.

Na dcada atual, h mais de 40 anos aps a

descoberta inicial, tem sido demonstrado que o

miofibroblasto reconhecidamente um elemento

central nos diversos tecidos, e que tem participa-

o ativa em diversos processos patolgicos

HISTOGNESE

Desde a primeira descrio dos miofibroblastos na

dcada de 70, vrias origens foram propostas para

estas clulas. Tendo em vista que a matriz extrace-

lular pode influenciar na diferenciao das clulas

do tecido conjuntivo, vrios tipos celulares deste

tecido poderiam se diferenciar em miofibroblastos,

tais como, fibroblastos, clulas musculares lisas,

pericitos e quaisquer outras clulas mesenquimais

indiferenciadas.

A heterogeneidade da composio do citoes-

queleto dos miofibroblastos levanta muitos ques-

tionamentos em relao origem destas clulas.

Os dados ultraestruturais fornecem evidncias de

que durante condies patolgicas e meios de cul-

tura, os fibroblastos e as clulas musculares lisas

vasculares adquirem aspectos morfolgicos muito

semelhantes aos dos miofibroblastos, o que suge-

re que estes dois tipos celulares possam ser pro-

genitoras dos miofibroblastos. Os filamentos inter-

medirios de alfa actina e desmina poderiam ser

oriundos de clulas musculares lisas ou pericitos,

uma vez que estas clulas apresentam uma dispo-

sio citoesqueltica similar. Uma possvel origem

vascular tambm foi proposta por Shum et al.(3)

com base em observaes morfolgicas, as quais

indicam a possibilidade de que as clulas miofibro-blsticas desmina positivas, migram da parede de

vasos sanguneos para o tecido.

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colgeno, a distino de miofibroblastos em rela-

o aos fibroblastos mais difcil.

ULTRAESTRUTURA

Os miofibroblastos compartilham aspectos mor-

folgicos em comum com fibroblastos e clulas

musculares lisas. Os fibroblastos em animais adul-

tos e humanos demonstram ncleo fusiforme, um

aparelho de Golgi bem desenvolvido, numerosas

cisternas de retculo endoplasmtico dilatadas,

mitocndrias esparsamente distribudas e micro-

filamentos, muitas vezes arrumados em discretas

bandas abaixo da membrana plasmtica. O contor-

no da clula geralmente bem delimitado e apre-

senta poucas extenses citoplasmticas.(7)

Em relao s clulas musculares lisas, suas

membranas plasmticas revelam numerosas pla-

cas, ou os chamados corpos densos associados

membrana, numerosas vesculas picnticas, e en-

volvimento por uma contnua lmina basal. Elas

possuem junes tipo gape junes de aderncia.

O citoplasma possui inmeras faixas de microfi-

lamentos usualmente dispostas paralelamente ao

longo eixo da clula, entre os quais pode-se ob-

servar numerosos corpos densos. Eles se caracte-

rizam como estruturas eletrodensas espalhadas

pelo citoplasma. O material desses corpos den-

sos parece ser similar ao material que forma as

bandas densas, as quais esto aderidas mem-

brana celular de certas clulas vasculares muscu-

lares lisas e provavelmente, correspondem s li-

nhas Z das fibras musculares estriadas. Em ambas

as estruturas, a alfa actina tem sido observada em

tcnicas utilizando imunohistoqumica. A fora de

transmisso do aparelho contrtil membrana ce-

lular de clulas musculares lisas ocorre atravs da

insero de filamentos de actina dentro das ban-

das densas.(8)

Os miofibroblastos exibem um contorno irregu-

lar com numerosas e longas extenses citoplas-

mticas e podem estar conectados por junes deaderncia e do tipo gap. Eles so envolvidos por

Segundo Gabbiani et al.,(1) os miofibroblastos

presentes em tecido de granulao so provavel-

mente originrios a partir de fibroblastos pr-exis-

tentes. Em tecidos de granulao estudados ex-

perimentalmente, os miofibroblastos expressam

temporariamente marcadores de diferenciao declulas musculares lisas, como, por exemplo, a

alfa actina, que desaparecem depois do fechamen-

to da ferida. Como nunca se constatou a presena

de msculo liso no interstcio de tecido de granu-

lao, seria pouco provvel concluir que os mio-

fibroblastos fossem derivados do msculo liso da

parede dos vasos. Nas alteraes relacionadas

injria, fenmenos de reparo, condies prolifera-

tivas e as presentes no estroma de neoplasmas, os

miofibroblastos expressam, em sua maioria, alfa

actina de msculo liso.

O destino dos miofibroblastos no bem defini-

do.(4)Somente fibroblastos tpicos so vistos nos

estgios finais dos processos fibrocontrteis, o que

sugere que o miofibroblasto pode alterar o seu ci-

toesqueleto e retornar condio de fibroblasto ou

desencadear o processo de apoptose.

MICROSCOPIA PTICA

Embora os miofibroblastos sejam melhor carac-

terizados na microscopia eletrnica, eles exibem

um padro histolgico que permite a sua identi-

ficao na microscopia ptica.(5) Eles so clulas

grandes, de aspecto fusiforme e frequentemente

estrelados, revelando longos prolongamentos cito-

plasmticos com um citoplasma acidoflico e fibri-

lar. O ncleo apresenta-se alongado, com aspecto

ovide e margens distintas. Segundo Filioreanu et

al.,(6) em seces finas com colorao adequada,

alguns ncleos podem se apresentar levemente

corados, com estriaes transversais proeminen-

tes. Um ou dois pequenos nuclolos acidoflicos

esto freqentemente presentes. Miofibroblastos

bem desenvolvidos so observados em reas com

pouca expresso de colgeno. Com o emprego damicroscopia ptica no estudo de reas ricas em

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uma lmina basal, possuem vrias vesculas pino-

cticas e apresentam-se conectados matriz extra-

celular por intermdio de fibronexus. Os fibronexus

so complexos transmembranares de microfila-

mentos intracelulares em aparente continuidade

com as fibras extracelulares de fibronectina. Estasestruturas so muito expressivas numericamente

nos miofibroblastos quando comparados s clu-

las musculares lisas. O citoplasma dos miofibro-

blastos exibe numerosos feixes de microfilamen-

tos (fibras de stress) usualmente arranjados

paralelamente ao longo eixo da clula, entre os

quais esto muitos corpsculos densos. O retcu-

lo endoplasmtico rugoso e o complexo de Golgi

apresentam-se bem desenvolvidos, ao passo que

o ncleo demonstra profundas invaginaes. Este

aspecto estrutural tem sido observado em vrios

modelos de contrao celular.

PAPEL BIOLGICO NACICATRIZAO

Os miofibroblastos so descritos em tecidos hu-

manos e animais durante condies normais ba-

seadas em estudos de ultraestrutura. Eles podem

ser observados no folculo ovariano e vilosidades

duodenais do rato, cpsulas das glndulas adre-

nais de ratos e camundongos, septo alveolar pul-

monar do macaco, ligamento periodontal de ratos

e camundongos e em muitos outros tecidos.(7)

Para se compreender a maneira pela qual os

miofibroblastos participam do processo de cica-

trizao, urge realizar um breve retrospecto dos

principais fenmenos relacionados com o proces-

so cicatricial. A cicatrizao um evento biolgico

complexo, o qual envolve inflamao, proliferao

celular e diferenciao. Est cada vez mais eviden-

te que a migrao, polaridade e reorientao das

clulas envolvidas neste processo, so influencia-

das pelos constituintes da matriz extracelular, prin-

cipalmente colgeno e fibronectina.(9) Uma das

etapas crticas da cicatrizao a formao do te-cido de granulao. O tecido de granulao con-

siste em muitas camadas de clulas fibroblsticas,

separadas por uma matriz colagenosa contendo

brotamento de capilares e clulas inflamatrias.

Os fibroblastos presentes no tecido de granula-

o, geralmente exibem aspectos ultraestruturais

de miofibroblastos.(10)Eles so bem numerosos e

mais desenvolvidos na camada exsudativa do feri-mento e vo sendo gradativamente substitudos a

partir da camada mais profunda, por fibroblastos.

Quando a matriz colagnica analisada, perce-

be-se a predominncia do colgeno tipo III, ao pas-

so que com a reabsoro do tecido de granulao

e fechamento do ferimento, os miofibroblastos de-

saparecem e um tipo mais rgido de colgeno pode

ser identificado. Em modelos experimentais, a an-

lise das protenas do citoesqueleto por mtodos deimunohistoqumica revela que os miofibroblastos

presentes no processo normal de cicatrizao nun-

ca expressam desmina ou miosina de msculo liso

durante o processo de fechamento da ferida. A di-

ferenciao em clulas semelhantes s musculares

lisas est ausente no tecido de granulao inicial.

Nesta fase, os miofibroblastos so pouco desenvol-

vidos, podendo expressar filamentos de vimentina

no seu citoesqueleto. A diferenciao dos miofi-

broblastos em clulas semelhantes s clulas mus-

culares lisas, se torna temporariamente aparente

quando os miofibroblastos comeam a expressar

alfa actina em quantidades cada vez maiores por

volta do 8 ao 15dia durante a cicatrizao. Esta

isoforma da actina desaparece progressivamente

dos miofibroblastos e deixa de ser detectada por

volta do 30dia.(7)

Durante o processo de cicatrizao, pode ocor-

rer um acmulo de quantidades excessivas de co-

lgeno ocasionando o aparecimento de cicatrizes

anormais, tambm denominadas quelides. A for-

mao de quelides parece ser uma predisposio

individual e, por motivos desconhecidos, mais

comum em negros.(9) Uma importante distino

deve ser feita entre a cicatrizao normal, a qual

caracterizada pela formao de um tecido slido

funcional e a cicatriz, que se forma s custas de ex-

cessivas quantidades de tecido de granulao. Es-tudos recentes salientaram a necessidade de um

equilbrio conveniente entre as concentraes de

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fatores de crescimento presentes na ferida duran-

te os diferentes estgios da cicatrizao.(10) Estes

trabalhos sugerem que uma produo excessiva de

tecido conjuntivo, provocando o aparecimento de

quelides, pode ser devido a um aumento nos n-

veis de TGF- 1.Atravs da secreo de citocinas inflamatrias,

quimiocinas, fatores de crescimento e mediadores

inflamatrios de natureza lipdica e gasosa, os mio-

fibroblastos desempenham um importante papel

na organognese, inflamao, reparo e fibrose da

maioria dos rgos e tecidos.(11)Gabbiani(12)desen-

volveu alguns estudos a fim de caracterizar o pa-

pel das citocinas e possveis fatores de crescimen-

to envolvidos na diferenciao de miofibroblastos.Conforme j foi salientado, a contrao da ferida

durante a cicatrizao mediada essencialmente

por miofibroblastos. A regulao da diferenciao

de miofibroblastos por parte das citocinas envolvi-

das no processo cicatricial, pode ser dependente,

entre outros fatores, da resistncia da matriz do te-

cido conjuntivo deformao.(13)A observao de

que o IFN-gdiminui a expresso de alfa actina de

msculo liso em clulas musculares lisas, sugere

que um fenmeno semelhante possa acontecer

em tecidos de granulao e tecidos com fibrose.

Desmoulire et al.,(14)demonstraram in vivoque o

IFN-gdiminui a expresso de alfa actina em fibro-

blastos em meio de cultura. Alm desses estudos,

outros estudos pilotos clnicos tem sugerido que a

aplicao do IFN-g eficiente na reduo de cicatri-

zes hipertrficas e leses fibromatosas.(15)

Aps o teste de muitas citocinas em um modelo

experimental consistindo em aplicao tpica das

mesmas em tecido subcutneo de rato, atravs de

uma mini bomba osmtica, foi demonstrado que

TNF, IL-1 e PDGF no estimulam a formao de

miofibroblasto, mesmo quando estas citocinas es-

to presentes na resposta tecidual granulomatosa,

ao passo que TGF- 1 e 2, e mais surpreendente

ainda o GM-CSF, estimulam regularmente o apare-

cimento de miofibroblastos ricos em alfa actina de

msculo liso.(16)TGF- 1 e 2 parecem exercer umpoderoso estmulo para a sntese de alfa actina, es-

timulando a diferenciao em fibroblastos cultiva-

dos.(14)

Considerando que a atividade pro-fibrtica do

TGF-btem sido amplamente descrita e particular-

mente estimula a sntese de colgeno tipo I,(17)al-

guns autores concluram que esta citocina pro-vavelmente muito importante no desenvolvimento

da cicatrizao e fibrose. Desmoulire et al.,(18)ob-

servaram que o TGF-bpode induzir a expresso de

alfa actina de msculo liso em fibroblastos dispos-

tos em meio de cultura sem soro, isto , na ausn-

cia de replicao celular, o que indica a sntese de

novo desta protena. Conforme salientado, o IFN-g

uma citocina multifuncional que tem sido utili-

zada como um agente teraputico em potencialpara o tratamento de vrias desordens fibrosas, in-

cluindo as cicatrizes anormais. Wang et al.(19) sa-

lientaram que, ao passo que TGF-b1 estimulava a

mudana fenotpica dos miofibroblastos, o IFN-g

alterava significativamente o citoesqueleto destas

clulas, atravs do declnio na expresso de alfa ac-

tina de msculo liso. Tal fato, implicava na dimi-

nuio da contratilidade dos miofibroblastos. Com

base nestas observaes, os autores sugeriram

que o IFN- gpode regular negativamente a ao do

TGF- bno controle das alteraes no fentipo de

miofibroblastos.

A ao do GM-CSF parece ser indireta, uma vez

que, quando esta citocina aplicada em meio de

cultura contendo fibroblastos, no h estmulo

para a sntese de alfa actina de msculo liso, ao

passo que miofibroblastos ricos em alfa actina so

observados depois da administrao local de GM-

-CSF em tecido subcutneo.(12)O mesmo fato pode

ser observado quando o GM-CSF aplicado quer

diretamente ou atravs de um vetor viral no alvolo

pulmonar.(20)Neste caso, a administrao de GM-

-CSF seguida pela expresso de TGF-b 1 e pela

expresso de colgeno e alfa actina. Estudos rea-

lizados mais recentemente tambm tem indicado

que a IL-10 poderia desempenhar uma funo es-

sencial na estimulao de miofibroblastos no rim.

(21) Todas estas evidncias podem sugerir que aaplicao local de GM-CSF poderia, quer direta ou

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indiretamente, atravs do acmulo de macrfagos

estimulados, contribuir para uma importante ex-

presso de TGF-b1, a qual por sua vez, induziria a

expresso de alfa actina e colgeno, resultando em

mudanas fibrticas ou cicatrizao.

Pesquisas adicionais tem revelado que a ao doTGF-b1 mediada atravs da poro ED-A da fibro-

nectina celular.(22)Esta concluso est baseada na

observao de que um anticorpo especfico para a

seqncia de ED-A inibe a ao de TGF-bem indu-

zir tanto a expresso de RNAm para alfa actina e

colgeno, bem como a expresso destas protenas.

Walker et al.(23)constataram que a IL-1 pode regu-

lar a expresso do receptor para o PDGF por parte

dos miofibroblastos presentes em pulmo de ra-tos. Karamichos et al.,(24)estudando o endotlio da

crnea de gatos, observaram que sob certas con-

dies patofisiolgicas, as clulas endoteliais po-

dem produzir colgeno anormalmente, em virtude

da ao estimulatria do TGF-b. Eles concluram

que as clulas endoteliais em proliferao adqui-

rem um fentipo temporrio de miofibroblastos.

Logo, o desenvolvimento dos miofibroblastos

provavelmente depende no s do estmulo forne-cido pela organizao da matriz extracelular, mas

tambm do efeito estimulatrio gerado por estas

citocinas descritas.

RESPOSTAS DO ESTROMA AOSPROCESSOS NEOPLSICOS

Muitos carcinomas invasivos e metastticos so

caracterizados por uma consistncia endurecidae retrao. Na maioria das vezes, eles encontram-

-se bem fixos aos tecidos adjacentes. Estas altera-

es so comuns em virtude da reao estromal

desmoplstica.

Ao que tudo indica, os miofibroblastos so par-

ticularmente numerosos dentro do estroma de

carcinomas metastticos e invasivos, e os fen-

menos de retrao observados so atribudos s

foras contrteis geradas pelos miofibroblastospresentes no estroma.(25)Isto sugere que a invaso

atravs da lmina basal necessria para desen-

cadear esta reao dos miofibroblastos do estro-

ma. Os miofibroblastos no esto uniformemente

presentes dentro dos carcinomas desmoplsicos.

Quando a sua disposio espacial em relao aos

outros componentes do estroma dos carcinomas

analisada, eles so mais evidentes no estromamesenquimal jovem, em reas que correspon-

dem a uma invaso primria do estroma, ou mais

consistentemente, na periferia da leso.(26)No cen-

tro da rea esclertica destes neoplasmas, os mio-

fibroblastos esto pobremente desenvolvidos ou

ausentes. Existem trs tipos de reao miofibro-

blstica do estroma observadas nos carcinomas

infiltrativos de ductos mamrios: a precoce, na

qual os miofibroblastos precedem s clulas carci-

nomatosas; a sincrnica, onde percebe-se que os

miofibroblastos aparecem espacialmente entre as

clulas do carcinoma; e a tardia, sendo possvel

encontrar os miofibroblastos dispostos mais cen-

tralmente em relao ao contorno perifrico das

clulas carcinomatosas. Estes trs tipos de rea-

o estromal podem ser observados em diferentes

reas dos carcinomas ductais, sendo que a mais

comum a reao sincrnica. Quando a matriz do

colgeno analisada, quantidades crescentes de

colgeno tipo III esto presentes, principalmente

no estroma recm formado; em contraste, o co-

lgeno tipo I mais evidente dentro da zona es-

clertica central dos carcinomas mamrios, reas

nas quais os miofibroblastos so substitudos por

fibroblastos.

Hinz(7) descreveram a ocorrncia de miofibro-

blastos tambm em sarcomas, nos quais eles ge-

ralmente constituem uma pequena frao da po-

pulao celular. Eles so bem identificados em

todos os casos de histiocitomas fibrosos malignos

e lipossarcomas esclerosantes bem diferenciados.

Embora eles se apresentem bastante numerosos

nas reas de desmoplasia, em nenhum dos exem-

plos citados, os miofibroblastos se constituem

nos elementos celulares dominantes de quaisquer

destes neoplasmas. Os miofibroblastos tm sido

identificados com menor freqncia e em menornmero em fibrossarcomas, sarcomas sinoviais,

hemangiopericitoma maligno e neuroblastoma.

7/24/2019 56ba5d9708ae6a0040adfd0c

8/9


123

Foram tambm descritos na Doena de Hodgkin

esclerosante nodular,(27)a qual apresenta uma rea-

o estromal nodular que altamente colageni-

zada. Estas reas contm numerosas clulas que

exibem o fentipo vimentina e actina ou apenas vi-

mentina, e poucos miofibroblastos com o fentipovimentina, actina e desmina.

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