Рис. 1. Графическое резюме обсуждаемой статьи в Cell. Потомство матерей, питавшихся жирной пищей (Maternal High-Fat Diet, MHFD), имеет измененную кишечную микробиоту (Dysbiosis), нарушенное (Impaired) социальное поведение, меньшее число производящих окситоцин нейронов в гипоталамусе (PVN — паравентрикулярные ядра гипоталамуса), а также пониженную синаптическую пластичность в вентральной области покрышки среднего мозга (VTA) в ответ на социальные стимулы. Всё это проходит, если искусственно заразить MHFD-мышей кишечными бактериями Lactobacillus reuteri

Потомство матерей, страдающих ожирением, имеет повышенный риск «расстройств аутистического спектра», включая нарушенное социальное поведение. Эксперименты на мышах показали, что в основе этих отклонений лежат изменения кишечной микробиоты. У мышей, чьи матери питались жирной пищей, снижается производство окситоцина в гипоталамусе, слабеет реакция «системы внутреннего вознаграждения» на социальные стимулы и, как следствие, пропадает интерес к общению. Оказалось, что все эти симптомы исчезают, если добавить мышам в пищу один-единственный вид кишечных бактерий — Lactobacillus reuteri.

Симбиотическая микробиота, в том числе кишечная, влияет на многие аспекты физиологии, поведения и эволюции животных (см. ссылки в конце новости). Состав кишечной микробиоты является отчасти наследственным (например, у млекопитающих бактерии эффективно передаются от матери к детям во время родов и при грудном вскармливании), отчасти зависит от контактов с другими особями и, конечно, от диеты.

С другой стороны, известно, что диета матери может влиять на неврологические и поведенческие характеристики потомства. В частности, у людей вероятность расстройств аутистического спектра повышается в полтора-два раза, если мать во время беременности имеет избыточный вес (см.: P. Krakowiak et al., 2012. Maternal Metabolic Conditions and Risk for Autism and Other Neurodevelopmental Disorders). Ранее было показано, что у мышей некоторые симптомы, характерные для аутизма (тревожность, стереотипные движения), можно ослабить, добавляя в пищу кишечную бактерию Bacteroides fragilis. Впрочем, на социальное поведение мышей и их интерес к общению с сородичами эта процедура не влияет (см.: Лечение дисбактериоза кишечника снимает симптомы аутизма, «Элементы», 13.12.2013). Эти данные позволяют предположить, что в основе связи между ожирением матери и аутизмом потомства могут лежать изменения кишечной микробиоты.

Нейробиологи и микробиологи из Медицинского колледжа Бейлора в Хьюстоне (США) решили проверить эту гипотезу экспериментально. Поскольку на людях проводить такие эксперименты невозможно, в качестве модельного объекта снова были выбраны мыши. Основное внимание в работе было уделено нарушениям социального поведения.

Для начала нужно было удостовериться, что у мышей, как и (предположительно) у людей, работает цепочка причинно-следственных связей «избыточное питание матери → ожирение → аутизм потомства». Для этого самок разделили на контрольную и опытную группы. Контрольных самок держали на стандартной диете, опытных — на диете с повышенным содержанием жиров. Как и ожидалось, это привело к ярко выраженному ожирению у самок в опытной группе.

Затем от всех самок было получено потомство, которое после трехнедельного периода грудного вскармливания в течение четырех недель кормили стандартной (нежирной) пищей. Потомство толстых матерей (Maternal high-fat diet, MHFD) не отличалось от потомства нормальных матерей (Maternal regular diet, MRD) по массе тела. Однако по своему социальному поведению они различались радикально: мыши MHFD (потомки перекормленных матерей) демонстрировали резко пониженный интерес к общению по сравнению с MRD (потомками нормально питавшихся матерей).

Социальное поведение тестировалось разными способами: например, двух незнакомых мышей сажали в камеру и подсчитывали число и длительность контактов. Дизайн другого теста показан на рис. 2.

Рис. 2. Тестирование на социабельность и интерес к незнакомцам. Тестируемую мышь сажают в камеру, подразделенную на три отсека проволочной сеткой, и дают немного освоиться (Habituation). Затем в левый отсек сажают другую мышь (M1), а правый оставляют пустым (E) и измеряют время, проведенное тестируемым животным около каждого из двух отсеков (тест на социабельность). После этого в правый отсек сажают еще одну мышь (M2) и смотрят, привлечет ли незнакомка повышенное внимание тестируемой особи (тест на социальную новизну). Изображение из обсуждаемой статьи в Cell

Мыши MHFD (потомки перекормленных матерей) во всех тестах показали нарушенное социальное поведение: они не хотели общаться с сородичами и не проявляли характерного для нормальных мышей повышенного интереса к незнакомцам.

Анализ микробиоты показал, что структура бактериальных сообществ в кишечнике мышей MHFD и MRD (потомков нормально питавшихся матерей) существенно различается, причем у их матерей эти различия примерно такие же. Теперь нужно было выяснить, существует ли связь между измененной кишечной микробиотой и нарушенным социальным поведением.

Мыши практикуют копрофагию, поэтому совместное проживание с другими мышами должно способствовать обмену кишечными бактериями между особями. Оказалось, что если юная мышь MHFD поживет в одном боксе с тремя мышами MRD 4–5 недель, то ее кишечная микробиота становится почти такой же, как у мышей MRD, а социальное поведение полностью нормализуется. В качестве контроля в данном случае использовались мыши MHFD, прожившие такое же время с тремя другими мышами MHFD (они так и остались социально ущербными). Этот результат согласуется с предположением о том, что изменение кишечной микробиоты у мышей MHFD является причиной нарушенного социального поведения.

Следующий вопрос — какие именно изменения микробиоты ответственны за асоциальность потомства перекормленных матерей. Может быть, у них в кишечнике живут какие-то особые бактерии, нарушающие поведение, а может, наоборот, у них не хватает каких-то микроорганизмов, обеспечивающих нормальное социальное поведение здоровых мышей. Авторы проверили, что будет, если три мыши MHFD поживут несколько недель с одной мышью MRD. Оказалось, что и в этом случае поведение MHFD нормализуется, а у мыши MRD оно остается нормальным. Значит, дело скорее всего в том, что в микробиоте асоциальных мышей MHFD чего-то не хватает, а не в том, что в ней присутствует что-то вредное.

В таком случае мыши, полностью лишенные бактериальной микробиоты (безмикробные), тоже должны быть асоциальными. Это было проверено и подтвердилось: безмикробные мыши показали во всех тестах на социальность примерно такие же результаты, как и MHFD. Более того, оказалось, что если искусственно «заразить» четырехнедельных безмикробных мышей микробиотой здоровых мышей MRD (путем скармливания помета), то их социальное поведение полностью нормализуется, так же как и состав кишечных бактерий. Этого, однако, не происходит, если такую же процедуру проделать с безмикробными мышами в восьминедельном возрасте (в этом случае состав кишечной микробиоты нормализуется, а социальное поведение — нет). Фекалии мышей MHFD, как и следовало ожидать, не обладают таким целительным действием, в каком бы возрасте их ни скармливали безмикробным мышам. Эти результаты согласуются с предположением о том, что микробиота как-то влияет на развитие мозга мышат.

Метагеномный анализ выявил несколько массовых видов кишечных бактерий, численность которых резко понижена у MHFD по сравнению с MRD. Сильнее всего (на порядок) сократилась численность бактерии Lactobacillus reuteri. Ранее было показано, что L. reuteri влияет на выработку окситоцина — важнейшего гормона, регулирующего социальное поведение (T. Poutahidis et al., 2013. Microbial Symbionts Accelerate Wound Healing via the Neuropeptide Hormone Oxytocin). Таким образом, начал прорисовываться возможный механизм влияния микробиоты на социальное поведение: жирная диета снижает численность L. reuteri у матерей и их потомства, это ведет к снижению производства окситоцина в мозге и, как следствие, к асоциальности.

Чтобы проверить эту гипотезу, авторы добавляли живых бактерий L. reuteri в воду, которой поили мышей MHFD в возрасте от 3 до 7 недель. В соответствии с ожиданиями, эта «биодобавка» нормализовала социальное поведение подопытных животных. На мышей MRD она не повлияла, очевидно, потому что у них и так есть достаточное количество L. reuteri в кишечнике. Мертвые бактерии L. reuteri от асоциальности не излечивают. Неэффективным оказалось и добавление в воду другого вида того же рода, L. johnsonii, численность которого тоже понижена у MHFD по сравнению с MRD.

У мышей MHFD и у безмикробных мышей, помимо асоциальности, наблюдаются и другие симптомы, характерные для аутизма: повторяющиеся действия и повышенная тревожность. Эти симптомы не исчезают ни от добавления L. reuteri в воду, ни от скармливания мышатам помета мышей MRD. С другой стороны, ранее было показано, что они снимаются добавлением в пищу человеческой кишечной бактерии Bacteroides fragilis (см.: Лечение дисбактериоза кишечника снимает симптомы аутизма, «Элементы», 13.12.2013).

Так или иначе, влияние L. reuteri весьма специфично: оно затрагивает только социальное поведение, но не другие компоненты «расстройств аутистического спектра», характерные для мышей с нарушенной кишечной микробиотой.

В полном соответствии с гипотезой о том, что L. reuteri влияет на социальное поведение через активацию окситоциновой системы мозга, у мышей MHFD оказалось пониженным число нейронов, производящих окситоцин, в паравентрикулярных ядрах гипоталамуса, отвечающих за производство окситоцина (при неизменном общем числе нейронов в этих ядрах). Добавление L. reuteri в питьевую воду нормализует количество выделяющих окситоцин нейронов.

Важнейшую роль в социальном поведении млекопитающих играет система внутреннего подкрепления, фундамент которой составляют дофаминэргические нейроны вентральной области покрышки среднего мозга (VTA) (см.: В «системе вознаграждения» найдены нейроны, возбуждающиеся от хороших предчувствий, «Элементы», 10.02.2012). Эти нейроны получают окситоциновые сигналы из паравентрикулярных ядер, что повышает их восприимчивость к другим сигналам (глутаматэргическим), несущим социально-значимую информацию. Попросту говоря, от окситоцина, приходящего в VTA из паравентрикулярных ядер, зависит интерес к сородичам и удовольствие, получаемое от общения с ними.

Анализ глутаматэргических возбуждающих постсинаптических токов в дофаминовых нейронах VTA показал, что у мышей MRD (потомков нормально питавшихся матерей) через сутки после десятиминутного общения с незнакомой мышью эти токи усилены по сравнению с MHFD (потомками перекормленных матерей). Через сутки после общения со знакомой мышью возбудимость этих нейронов одинаково низкая у MRD и MHFD. Таким образом, диета матерей влияет на силу долговременного ответа системы внутреннего вознаграждения на социальную новизну.

Наконец, в заключительной серии экспериментов авторы показали, что искусственное заражение мышат MHFD бактериями L. reuteri восстанавливает нормальное реагирование VTA на социальные контакты. Такой же эффект дает и простое закапывание мышам в нос окситоцина.

Таким образом, картинка получается вполне складная и убедительная. Диета с повышенным содержанием жиров приводит к ожирению и резко снижает численность L. reuteri в кишечнике самки. Мать передает свою нарушенную микробиоту потомству. Поскольку бактерии L. reuteri необходимы для нормального развития окситоцинэргической системы мозга, у такого потомства количество окситоциновых нейронов в гипоталамусе оказывается пониженным. Из-за этого система внутреннего вознаграждения (VTA) не учится генерировать приятные чувства в ответ на социальные стимулы, и животные вырастают безразличными к общению.

Механизм влияния L. reuteri на производство окситоцина паравентрикулярными ядрами еще предстоит выяснить. Однако есть веские основания полагать, что в этом задействован блуждающий нерв, который передает сигналы от кишечника в мозг, в том числе в паравентрикулярные ядра. Именно таким путем поступает в мозг информация о кишечных инфекциях, что стимулирует иммунную реакцию (X. Wang et al., 2002. Evidences for vagus nerve in maintenance of immune balance and transmission of immune information from gut to brain in STM-infected rats). Другой вид кишечных лактобацилл, L. rhamnosus, снижает беспокойство при стрессе, и в этом тоже участвует блуждающий нерв (если его перерезать, эффект исчезает). Наконец, есть прямые данные, указывающие, что L. reuteri влияет на производство окситоцина у мышей при посредничестве блуждающего нерва (T. Poutahidis et al., 2013. Microbial Symbionts Accelerate Wound Healing via the Neuropeptide Hormone Oxytocin).

Приложимы ли эти выводы к человеку? Очень может быть. Как уже говорилось, избыточный вес матери повышает вероятность «расстройств аутистического спектра» у людей. Известно, что у многих людей с такими расстройствами нарушена кишечная микробиота. Известно также, что ожирение сопровождается изменениями кишечной микробиоты у людей и других приматов. Поскольку L. reuteri излечивает «аутичных» мышат от асоциальности, а бактерия Bacteroides fragilis снимает другие симптомы, такие как повышенная тревожность и повторяющиеся действия, вполне можно допустить, что правильно подобранный комплекс кишечных бактерий может оказаться эффективным средством лечения симптомов аутизма не только у мышей, но и у людей.

Здесь можно еще порассуждать о том, что бактериям самим может быть выгодно стимулировать общительность своих хозяев и особенно интерес к незнакомцам, потому что это помогает бактериям заражать новых хозяев. Продолжая эту линию рассуждений, можно пофантазировать о возможной роли микробиоты в эволюции социального поведения в целом и отдельных его форм в частности, включая даже религиозные культы. Читателям, интересующимся подобными идеями, рекомендую статью Александра Панчина и его коллег: Alexander Y. Panchin, Alexander I. Tuzhikov and Yuri V. Panchin, 2014. Midichlorians — the biomeme hypothesis: is there a microbial component to religious rituals?.

Источник: elementy.ru

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